Printer Friendly

DIVERSITY AND EVOLUTION OF LIVING OYSTERS.

INTRODUCTION

Oysters are marine bivalve molluscs widely distributed in world oceans. Some oysters are keystone species for coastal and estuary ecology. They provide critical ecological services as filter-feeders, calcifiers, and sometimes reef-builders. Oysters are also important fishery and aquaculture species. They are highly abundant and have supported major fisheries and aquaculture industries in many countries. Oyster aquaculture, with an annual production of 5.6 million metric tons (FAO 2018), represents one of the most important mariculture industries in the world. Oyster populations have been on the decline because of overfishing, habitat destruction, and diseases (Beck et al. 2011). The protection and management of oyster resources require a good understanding of genetic diversity at both species and population levels. Genetic diversity is also a critical resource for genetic improvement and sustainable aquaculture of oysters (Guo 2009).

Genetic diversity is shaped by millions of years of evolution and critical for adaptation to changing environments. Oysters are remarkable in their tolerance to extreme environmental conditions, providing a good model species for studying stress adaptation. They are exceptionally well adapted to sessile life in estuaries, intertidal and shallow waters where environmental conditions fluctuate widely. Oysters can tolerate prolonged air exposure and extreme variations in salinity and temperature (Galtsoff 1964). They lack adaptive immunity but thrive in microbe-rich environments as filter-feeders. The remarkable resilience of oysters developed through adaptation to challenging environments is supported by their genomic diversity and complexity (Guo et al. 2015). Understanding the evolutionary history and diversity of oysters at genome, population, and species levels is central to all aspects of oyster biology.

Problems in oyster identification and classification have hindered the understanding of oyster diversity and evolution. Oysters are notoriously difficult to classify because of high plasticity in shell morphology. Oyster classification based on shell morphology has led to considerable confusions, both in classifying different ecotypes as different species and in failing to identify cryptic species (Harry 1985, Lam & Morton 2006). In the past two decades, molecular techniques have been applied to oyster classification and improved the understanding of oyster species diversity and taxonomy (Bayne 2017). Genetic and genomic studies have also provided insights into population and molecular diversities related to environmental adaptation. This article reviews progresses in the understanding of oyster diversity, classification, and evolution, with a focus on molecular studies of species and genome diversity, and the evolution of oysters in relation to environmental changes.

HIGHER LEVEL CLASSIFICATION

Oysters are bivalve molluscs that belong to class Bivalvia, subclass Pteriomorphia, order Ostreida, and superfamily Ostreoidea. Oyster classification began when Linnaeus described seven oyster species including three under the genus Ostrea (Linnaeus 1758). The genus Ostrea was broadly defined, and many bivalves across different families were once placed under Ostrea. A search of the World Register of Marine Species (WoRMS, http://www.marinespecies.org, accessed August 2018) for Ostrea returned more than 406 records. Most of these species do not belong to Ostrea as currently defined and have been assigned to other genera or families.

Families

Stenzel (1971) conducted a systematic study of fossil and living oysters. Based on shell morphology and anatomic characters, Stenzel classified extent oysters into two families, Gryphaeidae and Ostreidae (Table 1). In fossil records, both families appeared in Triassic without recognizable intermediate type. The apparent independence of the two Triassic lineages has led to the suggestion that the two oyster families might be diphyletic (Stenzel 1971). Phylogenetic analyses of molecular data supported the separation of the two families but not the diphyletic origin of Ostreoidea. In all analyses, Gryphaeidae and Ostreidae formed two distinct branches of a single mono-phyletic clade of oysters (Liu et al. 2011, Salvi et al. 2014, Raith et al. 2016, Salvi & Mariottini 2017, Fig. 1). Molecular analyses so far support the monophyly of Ostreoidea despite the missing link in fossil records. Although still controversial, oyster-like fossils have been identified from Late Permian (Nakazawa & Newell 1968, Mou & Liu 1993). It is likely that the two Triassic families are derived from a common ancestor in Permian, before the Permian-Triassic (P-Tr) mass extinction 252 Ma.

Subfamilies

Stenzel (1971) divided Gryphaeidae into three subfamilies: Gryphaeinae, Exogyrinae, and Pycnodonteinae. The first two subfamilies are extinct, and all living species are placed under Pycnodonteinae. Torigoe (1981) considered Gryphaeidae as a fossil-only family and elevated subfamily Pycnodonteinae to family Pycnodonteidae. Stenzel (1971) classified Ostreidae into two subfamilies, Lophinae and Ostreinae, both containing extent species. Torigoe (1981) moved Crassostrea and Saccostrea out of Ostreinae and established a new subfamily Crassostreinae (Table 1). Harry (1985) retained the subfamily of Pycnodonteinae under Gryphaeidae, accepted subfamily Crassostreinae under Ostreidae, and proposed several new genera under Ostreinae and Lophinae. As discussed in the following section, several genera proposed by Harry (1985) are not supported by molecular data. Lophinae. As discussed in the following section, several genera proposed by Harry (1985) are not supported by molecular data.

Within Ostreidae, molecular analyses revealed new phylogenetic structures that warrant taxonomic consideration. After analyzing 63 oysters with mitochondrial 16S ribosomal RNA (16S) and nuclear 28S ribosomal RNA sequences, Li (2013) found high levels of divergence between Crassostrea and Saccostrea and proposed that Saccostrea should be placed into a separate subfamily Saccostreinae Li (2013). Salvi et al. (2014) also noticed the significant divergence between Crassostrea and Saccostrea and the proposed subfamily Saccostreinae. The proposal by Li (2013) predated Salvi et al. (2014), and this review lists Li (2013) as the authority of the subfamily Saccostreinae (Table 1).

The species Striostrea were originally placed under the subfamily Ostreinae. Raith et al. (2016) found that Striostrea prismatica was highly diverged from other Ostreinae species in mitochondrial DNA sequences and proposed the new subfamily Striostreinae with the single genus Striostrea. The proposed Striostreinae is supported by another phylogenetic analysis of both mitochondrial and nuclear DNA sequences (Salvi & Mariottini 2017). Foighil and Taylor (2000) also showed that Saccostrea and Striostrea might not belong to Crassostreinae.

Subfamilies Lophinae and Ostreinae are well recognized by morphological characters (Stenzel 1971, Torigoe 1981, Harry 1985). In phylogenetic analyses, the two subfamilies of brooding oysters are often intertwined (Fig. 1), which led to the suggestion of combining the two subfamilies (Salvi et al. 2014, Raith et al. 2016). Within the large Ostreinae and Lophinae clade, the genera of Lophinae, Alectryonella, Dendostrea, and Lopha, are usually clustered together (Foighil & Taylor 2000, Salvi et al. 2014, Fig. 1), providing some genetic support for the subfamily Lophinae. Anatomically, Ostreinae species clearly differ from Lophinae species in their intestine looping around the stomach (Torigoe 1981, Li & Qi 1994). Taxonomy of Ostreinae and Lophinae is confusing (Fig. 1) and has not been adequately studied, and it may be premature to merge the two subfamilies. This review follows Stenzel (1971) and Harry (1985) in keeping the two subfamilies separate and accepts five subfamilies of Ostreidae: Crassostreinae, Lophinae, Ostreinae, Saccostreinae, and Striostreinae (Table 1).

Genera

In a comprehensive and radical reclassification of Ostreoidea, Harry (1985) established 12 new genera and subgenera (Table 1). Several reclassifications of Harry (1985) have been disputed by genetic analyses. Analyses of DNA sequences indicate that several genera proposed by Harry (1985), which are often monospecific, are embedded in Ostrea and should be reverted to Ostrea, including Cryptostrea, Myrakeena, Ostreola, Teskeyostrea, and Undulostrea (Lapegue et al. 2006, Shilts et al. 2007, Salvi et al. 2014, Raith et al. 2016, Li et al. 2017a). Genetic analysis also indicated that Parahyotissa should be changed to Hyotissa (Kirkendale et al. 2004). Huber (2010) considered Adontostrea, Eostrea, and Tiostrea as synonyms of Ostrea.

A major issue in the classification of Crassostreinae is the proposed new genus Magallana. Based on high genetic divergence between Asia-Pacific and Atlantic species of Crassostrea, Salvi et al. (2014) and Salvi and Mariottini (2017) proposed the new genus Magallana to include most Asia-Pacific species of Crassostrea. The proposal is opposed by many oyster biologists for its poor justification and disruption of a well-accepted genus (Bayne et al. 2017, Bayne et al. 2018). The genus Crassostrea is well established and contains many well-known species of ecological and economical significance. Genetic divergence between Asia-Pacific and Atlantic species of Crassostrea has been well recognized, including major differences in karyotype and mitochondrial gene order (Wang et al. 2004a, 2004b, Ren et al. 2010). Despite Asia-Pacific and Atlantic species showing high divergence in DNA sequences (Table 2), their protein sequences show a 99.2% cross-mapping identity (Zhang et al. 2014), and there are no major differences in shell morphology, anatomy, and biological characters to justify two genera. Sequence divergence should not be used as the sole justification for destructing a well-accepted genus. If the same level of divergence is used for establishing new genera, Crassostrea may be further broken down into more genera as a similar level of divergence is observed between Crassostrea virginica and Crassostrea columbiensis (Table 2). Duplication and rearrangement of mitochondrial RNA genes between Asia-Pacific and Atlantic species were cited as a justification for the new genus. Duplication and rearrangement of RNA genes are common, but the order of protein-coding genes (PCGs) is conserved at genus level in Crassostrea, Ostrea, and Saccostrea (Fig. 2). Variation among the three genera can be best explained by assuming the order in Ostrea as pleisomorphic, one transversion leading to Crassostrea and one transversion plus one translocation leading to Saccostrea.

In all phylogenetic analyses, Crassostrea is monophyletic (Liu et al. 2011, Salvi et al. 2014, Raith et al. 2016, Li et al. 2017a, Fig. 1), with the exception of Talonostrea talonata Li and Qi, 1994. The monospecific genus Talonostrea was proposed without the advantage of genetic data (Li & Qi 1994). Genetic analysis indicates that T. talonata is a sister species of Crassostrea zhanjiangensis Wu, Xiao & Yu, 2013 (Li et al. 2017a, Fig. 1). Li (2013) questioned the validity of T. talonata, and Li et al. (2017a) renamed the species as Crassostrea talonata (Li & Qi 1994), which has preserved monophyly of Crassostrea. It is not necessary or helpful to destruct the well-accepted Crassostrea with a new genus and rename many commercially important species. Naming Asia-Pacific oysters after Magellan is also unfortunate as he is associated with colonial rule in parts of Asia.

SPECIES DIVERSITY AND SPECIATION

Because of taxonomic confusions and inadequacies, the number of extent oyster species is not known. More than 100 extent oyster species have been reported by various authors, but some of these species may be synonymously applied to different ecotypes or shell forms. Harry (1985) recognized the significant influence of environmental conditions on shell morphology and accepted only 36 valid species. Huber et al. (2015) reported 77 species including 12 from Gryphaeidae and 65 from Ostreidae. The WoRMS database listed 78 accepted species (http://www. marinespecies.org, accessed August 2018). Recent genetic studies have clarified some taxonomic uncertainties, identified many new and cryptic species, developed diagnostic markers, and confirmed occurrences. This review finds 99 species or lineages of living oysters, although not all of which have been genetically confirmed or adequately characterized (Table 3). Limited DNA sequence data are available for only 73 species. In this review, available mitochondrial cytochrome c oxidase sub-unit I (COI) and 16S sequences were analyzed to highlight phylogenetic relationships (Fig. 1) and some of closely related species or species complexes (Table 2).

The sequence of COI is particularly informative on closely related species because of its relatively fast rate of divergence. A meta-analysis of COI divergence in 13,320 species pairs of animals has shown that 98.1% of species pairs has a divergence greater than 2%, with an average interspecific divergence of 11.3% (Hebert et al. 2003). Intraspecific divergences are mostly well below 1% and rarely higher than 2%. The divergence of Hebert et al. (2003) is measured in simple p-distance, which is slightly lower than the corrected Kimura 2-parameter (K2P) distance reported by most authors. For example, the average p-distance and K2P distance for 98 oyster COI sequence pairs are 2.53% and 2.62%, respectively. The difference is small and neglectable for most discussions. To be consistent, K2P distances are presented or recalculated in this review (Table 2). This review takes the proposition that if two lineages show a greater than 2% COI K2P distance and clear differences in geographic distribution, physiology, or other biological characters, they should be generally considered as closely related but independent species. Speciation is a continuous process, whereas classification is arbitrary. When classification is not straightforward, it is important to consider the phylogeography and biological characters of the species involved.

Pycnodonteinae

Twelve species of Pycnodonteinae have been reported and recognized (Table 3), several of which are worth noting. The species Pycnodonte taniguchii is considered a living fossil because it is the only living species of the otherwise fossil genus that was assumed to be extinct (Hayami & Kase 1992). This species lives in submarine caves off the Ryukyu Islands of Japan at a depth of 20-30 m. The species Neopycnodonte zibrowii is a deep-sea species found in northeastern Atlantic at a depth of 500-700 m (Wisshak et al. 2009). It is a large species (up to 300 mm) that may live for more than 500 y. It is similar to the giant Empressostrea kostini from the Spratly Islands of the South China Sea in having a perfectly straight hinge (Huber & Lorenz 2007). It is closely related to Neopycnodonte cochlear that is also found in northeastern Atlantic. The species N. cochlear is a deep-water species with a circumglobal distribution at low latitudes (Harry 1985). It is worth noting that extant species of this mostly fossil lineage are often found circum-globally in deep-sea or deep-water environments. The deep-sea environment may be essential for their long-term survival and wide distribution. From the point of genetic connectivity, circumglobal distribution of oysters is unusual and may require genetic scrutiny to determine if cryptic species exists.

Harry (1985) considered Hyotissa as monospecific with the circumtropical Hyotissa hyotis and erected Parahyotissa for four other species (mcgintyi, imbricata, quercinus, and numisma). The new genus is not supported by genetic analysis (Kirkendale et al. 2004). Eight Hyotissa species are recognized based on shell morphology and distribution, although three of them have not been confirmed by genetic data (Table 3). It has been shown that H. hyotis from the Florida Keys of the United States is a recent introduction from the Indo-Pacific (Bieler et al. 2004). The 16S sequences of H, hyotis are highly divergent (1.7%-6.6%) and may contain three different species (this study).

Crassostreinae

Crassostreinae contains about 26 species, including some possible synonyms that have not been genetically confirmed: Crassostrea tulipa, Crassostrea cuttackensis, Crassostrea aequatorialis, and Crassostrea iredalei (Table 3). The species Crassostrea iredalei is considered as a junior synonym of Crassostrea bilineata, but it is also genetically diverse. Among available COI sequences of C. iredalei, K2P distances between some sequences are as high as 2.6%-3.5% (Table 2). Considering the distance between Crassostrea gigas and Crassostrea angulata is about 2.2%-3.6% (Wang et al. 2010), "C. iredalei" may include more than one species. Further genetic analyses are needed before assigning all C. iredalei to C. bilineata. Oysters C. iredalei and Crassostrea madrasensis are clearly two different species as their COI K2P distances are as high as 5.5%. Genetic analyses have synonymized Crassostrea gasar and Crassostrea paraibanensis under Crassostrea brasiliana (Lapegue et al. 2002, Huber 2010, Lazoski et al. 2011), Crassostrea rivularis (red meat) under Crassostrea ariakensis (Wang et al. 2004a), and C. rivularis (white meat or C. sp. Li & Qi 1994) under Crassostrea hongkongensis (Lam & Morton 2003, Wang et al. 2004a). The species Crassostrea corteziensis is genetically confirmed as occurring in the Gulf of California, Mexico (Raithetal. 2016).

Genetic analyses have identified several new and cryptic species of Crassostrea including Crassostrea dianbaiensis (Xia et al. 2014), Crassostrea zhanjiangensis (Wu et al. 2013), Crassostrea gryphoides tanintharyiensis sp. nov., and Crassostrea gryphoides dwarkaensis sp. nov. (Li et al. 2017b). Li et al. (2017b) identified Crassostrea gryphoides tanintharyiensis sp. nov. based on a specimen from Tanintharyi, Myanmar (submitted to Marine Biological Museum of the Chinese Academy of Sciences, Institute of Oceanology, Qingdao). Based on samples from Dwarka, India, Crassostrea gryphoides dwarkaensis sp. nov. was previously identified as C. gryphoides (Reece et al. 2008), a fossil species that became extinct about 3 million years ago (Harzhauser et al. 2016). These two subspecies have a COI K2P genetic distance of 2.1%, which is similar to the distance between Crassostrea gigas and Crassostrea angulata, 2.2%-3.6% (Wang et al. 2010, Table 2). The low genetic divergence suggests that these subspecies pairs diverged recently. It is possible that C. g. dwarkaensis and C. g. tanintharyiensis evolved from the extinct C. gryphoides.

Oysters Crassostrea gigas and Crassostrea angulata provide a good example of two closely related subspecies or species. They have been regarded as conspecific by some researchers because of their morphological similarities, ability to hybridize easily, and low divergence as measured with allozyme markers (Menzel 1974, Buroker et al. 1979, Huvet et al. 2004, Bayne 2017). Clear genetic divergence has been demonstrated by DNA sequence analysis, which has led to the recognition of separated species by some (Lapegue et al. 2004, Liu et al. 2011) but not all (Reece et al. 2008) authors. Wang et al. (2010) regarded them as subspecies as their COI K2P distance, 2.2%-3.6%, is higher than most intraspecific distances but lower than most interspecific distances. Considering that C. gigas and C. angulata are mostly allopatric and have different biological characteristics, they should be considered as two closely related subspecies or species. Similarly, Crassostrea talonata oysters from China and Peru likely represent two separate species as their COI K2P distance is 3.6% (Li et al. 2017a). Furthermore, C. talonata oysters from China may not be conspecific as their COI divergence is as high as 3.3% (Table 2).

Genetic markers have been developed and used for rapid and effective identification of oyster species (Klinbunga et al. 2003, 2005, Cordes et al. 2008, Wang & Guo 2008a, 2008b), which have contributed to the understanding of the true distribution of oysters. For example, according to traditional classification, Crassostrea ariakensis or Crassostrea rivularis has a wide and abundant distribution along the coast of China (Zhang & Lou 1956, Li & Qi 1994). Analysis with genetic markers could only confirm low occurrence at few sites, suggesting that the abundance and wide distribution based on traditional identification are incorrect or the populations have greatly declined (Guo et al. 2006, Guo et al. 2008a). Either way, the low abundance and isolated distribution confirmed by genetic markers indicate that Crassostrea ariakensis in China should be protected as an endangered or threatened species.

Saccostreinae

Saccostrea species are small- to medium-sized rock oysters widely found on rocky shores of the Indo-Pacific. Because of their small size and close attachment to rocks, shells of Saccostrea are extremely variable, making classification particularly difficult. Stenzel (1971) recognized the shell diversity and complexity of Saccostrea species and regarded cucullata (Born. 1778) as a superspecies that included all Saccostrea species from Indo-Pacific, including Saccostrea glomerata and Saccostrea mordax. Harry (1985) went further by accepting S. cucullata as the only valid Saccostrea species from Indo-Pacific and Saccostrea paltnula (Carpenter, 1857) as the only other species from eastern Pacific.

Further analyses of shell morphology and anatomical characters identified seven different species from Japan and China: Saccostrea echinata, Saccostrea glomerata, Saccostrea kegaki, Saccostrea malabonensis, Saccostrea mordax, Saccostrea cucullata, and Saccostrea mytiloides (Torigoe 1981, Li & Qi 1994, Xu 1997). Detailed anatomic analyses provided support for S. cucullata, S. glomerata, S. echinata, Saccostrea palmula, and S. mordax (do Amaral & Simone 2016). Lam and Morton (2006) analyzed 16S sequences of rock oysters from Indo-Pacific and identified S. glomerata, S. kegaki, two lineages of S. mordax (A and B), and seven lineages of S. cucullata (A-G). Hamaguchi et al. (2014) discovered a third lineage of S. mordax (C) and two lineages of S. malabonensis. Sekino and Yamashita (2016) identified three additional non-mordax lineages of S. cucullata (H-J). Lineage S. cucullata F has been tentatively assigned to S. malabonensis, S. cucullata H to S. echinata, and S. cucullata J to Saccostrea spathulata (Sekino & Yamashita 2016, Li et al. 2017b). Although most S. cucullata lineages cannot be confidently assigned to nominal species, they are highly divergent and likely represent independent species. The S. mordax lineages are highly diverse and contain at least two species with lineage C very different from lineages A and B. The COI K.2P distance between lineages A and B is 1.5%-2.3%, but their distance from lineage C is 9.3%-10.7% (Table 2). These findings highlight the high species diversity of Saccostrea species and the challenges of classifying them.

Genetic analysis has confirmed that Saccostrea commercialis is synonymous with Saccostrea glomerata (Anderson & Adlard 1994), but the eastern Pacific Saccostrea palmula is distinct from Indo-Pacific species (Hamaguchi et al. 2014, Raith et al. 2016).

Ostreinae

Taxonomic status of flat oysters Ostrea stentina, Ostrea equestris, Ostrea aupouria, and Ostrea spreta has been controversial not only because of their close relationship but also because of their wide geographic distributions. Harry (1985) synonymized O. spreta and O. equestris from western Atlantic but considered the eastern Atlantic O. stentina as an independent species based mostly on their geographic separation. Molecular analysis has indicated that O. equestris from America is closely related with O. aupouria from New Zealand (Kirkendale et al. 2004). The species Ostrea equestris has also been reported from Pacific side of central America (Raith et al. 2016). Shilts et al. (2007) analyzed COI, 16S, and ITS1 (intergenic spacer 1 of major rRNA genes) sequences and concluded that O. equestris of America, O. aupouria of New Zealand, and O. stentina of Mediterranean and eastern Atlantic were part of the global distributed O. stentina. Salvi et al. (2014) also suggested that O. stentinajequestris/aupouria/spreta may represent a single taxon. Hamaguchi et al. (2017) identified O. stentina in Japan, recognized significant divergence, and regarded these lineages or species as the O. stentina complex. Analysis of available COI sequences indicates that the O. stentina complex is heterogenous and contains three lineages. The three lineages differ by 3.6%-5.4% in K2P distance (Table 2) and likely represent three different species. One of the three species is O. equestris from Atlantic and Pacific coasts of the United States and Mexico, which WoRMS listed as a synonym of O. stentina. The identity and distribution of the other two species, which are referred to as O. stentina A and B (Table 3), require further studies.

Another closely related species pair indicative of recent divergence is Ostrea lurida and Ostrea conchaphila from eastern Pacific. They were considered conspecific based on morphological characters (Harry 1985, Coan et al. 2000). Molecular analyses revealed clear genetic differences in support for separate species (Poison et al. 2009, Raith et al. 2016). The COI K2P distance between O. lurida (n = 2) and O conchaphila (n = 68) ranged from 3.6%-4.7%, higher than that between Crassostrea gigas and Crassostrea angulata (Table 2). Furthermore, O. lurida and O. conchaphila do not overlap in geographic distribution occurring in the north and south of Punta Eugenia in Baja California, Mexico, respectively.

Western Atlantic Ostrea permollis from Florida, and Ostrea puelchana from Argentina are another species pair showing low or recent genetic divergence (Shilts et al. 2007, Salvi et al. 2014). The COI K2P distance between the pair is 2.2%-3.8% (Table 2), which is almost identical to the level of divergence found between Crassostrea gigas and Crassostrea angulata (Wang et al. 2010). The European flat oyster Ostrea edulis and Australia flat oyster Ostrea angasi are considered conspecific based on low divergence in ITS sequence (Kenchington et al. 2002). The Australian flat oysters may represent a recent colonization event that is at early stages of divergence and speciation (Hurwood et al. 2005). The COI K2P genetic distance between O. edulis and O. angasi is 1.3%-2.9%, which may qualify them as two subspecies or species.

Recent and Ongoing Speciation

As discussed earlier, genetic analyses have revealed a surprisingly large number of species pairs or complexes showing low or recent divergences. The COI K2P genetic distance between species pairs is typically 2%-4% (Table 2), which is on the borderline between species and subspecies. This review considers that lineages showing greater than 2% K2P distance and differences in distribution or biological characters are different species or subspecies. It may be genetically more appropriate to designate some of the closely related species as subspecies as in the case of Crassostrea gigas gigas and Crassostrea gigas angulata (Wang et al. 2010). This review did not list them as subspecies for taxonomic stability and simplicity.

The divergence rate of COI in invertebrates is estimated as 1.23% (P2K) per million years (Wilke et al. 2009). Applying the 1.23%/million year divergence rate to oysters produces divergence time estimates at 1.8-2.7 Ma for Crassostrea gigas and Crassostrea angulata, 2.2 Ma for Crassostrea gryphoides dwarkaensis and Crassostrea gryphoides tanintharyiensis, 2.9 Ma for Crassostrea talonata of China and Peru, 3.0-3.9 Ma for Ostrea stentina and Ostrea equestris, 2.9-3.8 Ma for Ostrea conchaphila and Ostrea lurida, 1.8-3.1 for Ostrea permollis and Ostrea puelchana, and 1.6 Ma for Saccostrea mordax A and B. The divergence time between Ostrea conchaphila and Ostrea lurida based on 16S is about 1.5-3.9 Ma, and the upper limit is almost the same as the COI estimate of 3.8 Ma. Analyses of all mitochondrial protein-coding genes placed the divergence time between C. gigas and C. angulata at 2.7 Ma (Ren et al. 2010), which is the same as the upper limit estimated with COI. These findings suggest that oysters experienced active speciation during the past 3^1 million years.

Recent speciation may not be limited to oysters as species complexes have been observed in other bivalve molluscs. For example, the divergence time for the Meretrix petechialis species complex is estimated as 2.0-3.6 Ma (Wang et al. 2017a) and the divergence time for Mytilus edulis and Mytilus galloprovincialis is estimated as 2.5 Ma (Ren et al. 2010). It is possible that oysters and some other bivalves expanded 3-4 Ma and subsequent changes in marine environment led to isolation and divergence, resulting in closely related species and species complexes.

Ongoing speciation is supported by exceptionally high levels of intraspecific divergence in some species (Table 2). In Crassostrea virginica, populations from the Atlantic and Gulf coasts are genetically distinct with a break and steep cline in southern Florida (Hare & Avise 1996). Their COI divergence is 2%-2.2% (Wang et al. 2010), which is exceptionally high for intraspecific divergence and may qualify them for subspecies status. Other species showing high intraspecific diversity include Crassostrea iredalei, Crassostrea talonata, Ostrea permollis, and Ostrea puelchana (Table 2). These species may be experiencing ongoing speciation, and some of them such as C. virginica, C. iredalei, and C. permollis may have diverged into different subspecies. The north and south populations of Crassostrea ariakensis along the coast of China are also genetically distinct and shared no haplotypes in mitochondrial DNA. They have diverged by about 1.02 million years as estimated with whole mitochondrial genome data (Ren et al. 2016). These findings support recent and ongoing speciation of living oysters.

MOLECULAR DIVERSITY AND ADAPTATION

Genomic Diversity and Complexity

Oysters are known to have high genetic diversity or polymorphism at the molecular level (Hedgecock et al. 2005, Guo et al. 2008b). Early studies have shown that the Pacific oyster has a single nucleotide polymorphism (SNP) frequency of one in 75 bp or 1.33% (Fleury et al. 2009). The SNP frequency in the eastern oyster is even higher, 2%-5% at the population level (Zhang & Guo 2010, Eierman & Hare 2014). Whole genome sequencing has confirmed high polymorphism in the Pacific oyster (Zhang et al. 2012). The frequency of SNPs and indels in a wild Pacific oyster is 1.3%, which is 9.3 times that of a human being (Zhang et al. 2012, Guo et al. 2015). The sequencing of the Pacific oyster genome has also revealed other diversities and complexities in addition to sequence polymorphism. The Pacific oyster genome contains 36.1 % repetitive sequences including large numbers of miniature inverted-repeat transposable elements (157,007 copies or 8.8% of the genome), some of which may still be active (Zhang et al. 2012).

The Pacific oyster genome contains 28,027 protein-coding genes (Zhang et al. 2012) and the eastern oyster genome contains 34,596 protein-coding genes (McDonnell Genome Institute 2017). Other sequenced bivalve genomes also contain large numbers of protein-coding genes: 26,415 in Patinopecten yessoensis (Wang et al. 2017b), 28,602 in Chlamys farreri (Li et al. 2017c), 32,937 in Pinctada fucata martensii (Du et al. 2017), 36,549 in Modiolus philippinarum, and 33,584 in Bathy-modiolusplatifrons (Sun et al. 2017). In comparison, the human genome has about 19,000 protein-coding genes (Ezkurdia et al. 2014). The fact that oysters and other bivalves have more protein-coding genes than humans is interesting and attests their high gene diversity.

In Pacific oyster, many gene families related to stress and immune response are greatly expanded, and genes of the expanded families show exceptionally high diversity in sequence, domain structures, and expression profile (Zhang et al. 2012, Guo et al. 2015, Zhang et al. 2015). For example, the Pacific oyster has 88 heat shock protein 70, 48 inhibitor of apoptosis (IAP), and 83 toll-like receptors, compared with 17, 8, and 10, respectively, in humans. Heat shock proteins protect cellular components during stress, whereas IAP prevents cells from apoptosis (Zhang et al. 2012). Toll-like receptors are key immune receptors for pathogen recognition. Sequence and domain structure of these expanded genes are highly diverse compared with that in vertebrates. The expanded and diversified genes show different expression profiles under different environmental conditions (He et al. 2015, Zhang et al. 2015). The expansion of stress response genes and associated high sequence, and structural and functional diversity may be central to the adaptation of oysters to highly stressful and widely changing environments (Guo et al. 2015). The expansion and diversification of immune response genes may increase the specificity and complexity of the innate immune system that are critical to the adaptation of oysters to life as a filter-feeder in microbe-rich environments (Guo & Ford 2016). The expansion of these stress and immune response genes is shared by some other bivalves such as pearl oyster, mussel, and scallops (Du et al. 2017, Li et al. 2017c, Wang et al. 2017b), suggesting that the expansion occurred early in bivalve evolution and probably maintained by similar interactions with the environment in different groups of bivalves.

Karyotype Evolution

Extent oysters have a conserved karyotype. All oysters studied so far have a haploid number of 10 chromosomes, whereas the dominant karyotype of clams and scallops has a haploid number of 19 (Wang & Guo 2004). The genome size of oysters is also about half of that of scallops and clams (Hinegardner 1974, Zhang et al. 2012, Wang et al. 2017b), which has raised the question whether there was a genome duplication event during bivalve evolution with oysters representing the diploid lineage (Wang & Guo 2004). The fact oysters emerged later than most clams and scallops in fossil records supports the alternative hypothesis that the oyster genome may represent a degenerated karyotype from an ancestor with 19 chromosomes. It is likely that the common ancestor of most extent bivalves had a haploid number of 19 chromosomes. Chromosome loss occurred during evolution, leading to oysters (n = 10), pearl oysters and mussels (n = 14), and some scallops (n = 13, 14, 16). The karyotype of Yesso scallop (n = 19) shows remarkable macrosynteny with the hypothetical karyotype of the bilaterian ancestor (n = 17) (Wang et al. 2017b). The scallop genome also shows unprecedented conservation of bilaterian gene families. The loss of chromosomes in oysters, pearl oysters, and mussels could be an adaptation to sessile life. It may also explain why oysters can tolerate polyploidy well (Guo et al. 2009). Most of the bivalve genomes sequenced so far do not have good chromosomal-level assembly. As genome assembly improves, comparative genome analysis may provide insights into the role of chromosome loss and rearrangements in the evolution of oysters.

Genetic Diversity, Adaptation, and Balancing Selection

Marine species usually have large and well-connected populations with low divergence across wide geographic range (Palumbi 1994). As typical marine bivalves, oysters have high fecundity and planktonic larvae that are capable of longdistance dispersal. As expected, genetic differentiation among geographic populations is generally low in oysters. The detection of population structure depends on the type of genetic markers used. Early studies with allozyme markers revealed little genetic differentiation among oyster populations (Buroker et al. 1979, Buroker 1983). Analyses with DNA markers have revealed a clear breakpoint between eastern oyster populations from the Gulf and Atlantic coasts of the United States (Karl & Avise 1992, Hare & Avise 1996). The failure of allozyme markers to show existing genetic structure may indicate that these markers are not neutral and their variation is shaped by balancing selection.

Selection has been demonstrated to act on genetic variation and affect population structure in oysters. In Delaware Bay, eastern oysters face differential selection by diseases with high prevalence in the lower bay and little or no disease in low-salinity areas in the upper bay. Population structure corresponding to disease prevalence was detected with marker linked to disease resistance, but not with neutral markers, suggesting selection by diseases contributed to genetic differentiation (Hofmann et al. 2009, Guo et al. 2012). Selective breeding has led to rapid improvement in disease resistance (Ford & Haskin 1987, Calvo et al. 2003, Guo & Ford 2016). In the Pacific oyster, finescale population structure, coinciding with divergence in growth, physiology, heat tolerance, and gene expression, has also been detected in a relatively small region with genome-wide SNPs (Li et al. 2018). These results suggest that selection and local adaptation may be pervasive in oyster populations. Selection may vary spatially or temporally depending on environmental changes, creating an overall effect of balancing selection.

Balancing selection is likely a major force in shaping genetic variation in oysters and other marine bivalves. Strong balancing selection may be the primary reason why high levels of genetic diversity in sequence, domain structure, and function are maintained in oysters (Guo et al. 2015). With planktonic larvae capable of wide dispersal and a sessile adult stage that cannot move or use avoidance, oysters must rely on high genetic diversity and/or plasticity to coup with unpredictable and wildly fluctuating environmental conditions. Larvae produced at a low salinity site may disperse and settle at high salinity sites. Balancing selection would retain alleles favored by both low and high salinity environments and therefore maintains genetic diversity. Balancing selection in oysters may be particularly strong because (1) oysters have very different larval and adult stages that alleles having high larval fitness may not perform well during adult stage; (2) oyster larvae are capable of long-distance dispersal and may settle in diverse environments; and (3) oysters live in estuaries and coastal seas, intertidally or in shallow waters, where environmental conditions vary greatly. Environmental heterogeneity in time and space creates balancing or multidirectional selections that favor genetic diversity. The high fecundity of oysters allows them to tolerate high genetic diversity (or genetic load) and high larval mortality (Launey & Hedgecock 2001, Li & Guo 2004, Plough 2016). Variation in reproductive success (Hedgecock 1994) along with long-distance dispersal may also disrupt directional selection and favor the retention of genetic diversity.

EVOLUTIONARY HISTORY AND ENVIRONMENTAL CHANGE

The origin of oysters is still obscure. The oldest true oyster fossil was Liostrea of Gryphaeidae from Early Triassic about 252 Ma (Hautmann et al. 2017). The Liostrea species were found attached to Ammonoids at the shores of Pangea Sea (Greenland), the Salt Range (Pakistan), and Spiti (India), living in open euhaline waters. They probably gave rise to Gryphaea of the Gryphaeidae lineage. Oysters of Ostreidae such as Umbos-trea and Lopha appeared around the same time or about 5 million years later (Marquez-Aliaga et al. 2005). Early Gry-phaeid species (Liostrea and Gryphaea) probably preferred euhaline, cool, and deep/calm soft bottoms in the Triassic Arctic realm, whereas early Ostreid species lived in warm euhaline waters of the Triassic Mesogean and Pacific realms (Stenzel 1971, Hautmann et al. 2017). The sudden appearance of two oyster families in Early Triassic suggests that they may be derived from a common ancestor in Permian and experienced rapid divergence. On the east shores of the Paleo-Tethys Ocean, in what is now southern China and Japan, Lopha-like oysters were observed from Late Permian about 260-275 Ma (Nakazawa & Newell 1968, Mou & Liu 1993, Fig. 3). It is generally accepted that true oysters attach to their substrate sinisterly. Although those Lopha-like oysters share some of the unique characteristics of Lopha, their attachment to substrate, whether sinisterly, dextrally, ambivalently, or free-living, is uncertain, making their relationship to true oysters controversial. Nevertheless, it is likely that the two oyster families originated from Late Permian. We may have to entertain the possibility that early oysters attached ambivalently or free-living.

The emergence of oysters coincided with the P-Tr mass extinction 252 Ma that wiped out more than 90% of the marine species (Erwin 1994). The rise of oysters is likely part of the bivalve takeover of the nearshore benthic environment that was dominated by Rhynchonelliform brachiopods before the P-Tr extinction (Fraiser & Bottjer 2007). The P-Tr mass extinction has been attributed to complex environmental changes that may include volcanic eruption, ocean regression, global warming, ocean anoxia, acidification, and increased levels of hydrogen sulfide. Anoxia, in particular, may have contributed to the rise of oysters and other bivalves that were more tolerant to these conditions (Wignall & Hallam 1992). The expansion of genes related to stress response such as heat shock protein 70 and IAP might have contributed to the survival of oysters and other bivalves over anoxia and other stressors during the mass extinction. After the initial rise in Triassic, escalating predatorprey interactions during the Mesozoic Marine Revolution (Vermeij 1977, Harper & Skelton 1993) might have further favored oysters and bivalves with large and strong shells, leading to the development of modern marine fauna.

After the P-Tr mass extinction, the abundance or diversity of oyster fossils increased rapidly, amid large fluctuations, and reached the highest point in Late Cretaceous, 66-72 Ma (Fig. 3). Although fossil records are incomplete and sometimes uncertain, the fluctuation in the abundance of oyster fossils is likely real as it is correlated with that of Pectinidae, epibenthic filter-feeders of the same subclass. The correlation between the two groups of bivalves indicates similar interactions with environmental changes, whereas the divergence may suggest differential response to changing environments because of their biological differences.

Triassic-Jurassic mass extinction and Cretaceous-Paleogene (K-Pg) mass extinction are reflected in two major declines in the abundance of oysters and scallops (Fig. 3). Although the cause for the Triassic-Jurassic extinction is less clear, the K-Pg extinction is probably caused by the impact of a massive asteroid 66 Ma that greatly changed the global environment and reduced photosynthesis (Schulte et al. 2010). Before K-Pg extinction, warm climates and elevated sea level in Late Cretaceous (Miller et al. 2005) may have contributed to the high abundance and diversity of oysters (Fig. 3). After the asteroid impact, the reduction in phytoplankton, increase in acidity, and drop in ocean temperature might be responsible for mass extinction and the great decline of oysters and scallops from 65 to 60 Ma. Several pairs of Crassostrea species diverged in Asia about 43-16 Ma after the K-Pg extinction (Ren et al. 2010). The importance of ocean regression or the loss of shallow epicontinental seas in marine mass extinctions has been recognized (Ager 1976, Hallam 1989). The loss of shallow sea environments may be particularly detrimental to oysters and other bivalves that mostly lived in intertidal or shallow-water environments. Most of the early oysters were distributed in the northern hemisphere (Fig. 3), a pattern that is mostly retained in extend species (Table 3).

Environmental change is a key driver of evolution. Identifying past environmental factors that affected oyster diversity and abundance is challenging but critical to the understanding of the biology and evolutionary trajectory of extent species. Fossil records show a peak of oyster abundance and diversity at 4 Ma, which declined and reached a low point at 2 Ma (Fig. 3). The climate of the last 3 million years is characterized by glacial and interglacial cycles of deepening ice ages (Lambeck et al. 2002). The expansion of oysters 4 Ma followed by intensified ice ages may be a contributing factor to the recent speciation of oysters during the past 3-4 million years. Since the last glacial maximum about 20,000 y before present (BP), the sea level has risen by about 130 m (Lambeck et al. 2002). The massive Holocene oyster reefs on the western shores of Bohai Sea, China, flourished after rapid ocean transgression that peaked around 6,000 y BP (Jia & Tian 1996, Fan et al. 2005, Liu et al. 2016). Between 6,500 and 2,300 y BP, salinity gradually increased from 20 to 30, and climate change after 4,100 y BP, especially aridity, loss of vegetation cover, and increased silt deposition from rivers, probably led to the demise of the oyster reefs (Hong et al. 1995). The rise and fall of Holocene oyster reefs in the Bohai Sea support the importance of ocean transgression and climate change for the survival and evolution of oysters.

In summary, molecular studies of living oysters have revealed high levels of genetic diversity at species, population, and genome levels. Many new and cryptic species have been discovered, revealing surprisingly high species diversity under similar shell morphology. Genetic analyses identified several closely related species or species complexes where low genetic divergence points to recent or ongoing speciation during the past 3-4 million years. The Pacific oyster genome is highly polymorphic and gene-rich, with extensive expansion of genes related to stress and immune response. The expansion and diversification of stress and immune response genes may be central to the adaptation of oysters to highly stressful and dynamic environments. Local adaptation in oysters may be pervasive but countered by high gene flow and balancing or multidirectional selections that favor genetic diversity. Oysters have experienced several expansion and contraction events because of climate change since their origin in Permian.

Despite recent progresses, molecular classification and phylogeny of living oysters are still at early stages. Many taxonomic uncertainties exist and many species have not been subjected for adequate genetic analysis. New and cryptic species are still to be discovered and characterized. There is a great need for a global survey of living oysters and a comprehensive analysis of both genetic and morphological data. Studies on molecular adaptation to environmental change may provide insights into the evolution and speciation of oysters.

ACKNOWLEDGMENTS

The publication is dedicated to Dr. Susan E. Ford (1942-2017), a world-renowned shellfish pathologist and beloved colleague who had a great impact on the field of oyster biology including the work cited in this study. The authors thank Zhenwei Wang and Michael Whiteside for their comments. This study is partly supported by USDA NIFA award (2015-70007-24245), NJAES Project 1004475/NJ32920, and National Science Foundation of China (No. 41776179).

LITERATURE CITED

Ager, D. V. 1976. The nature of the fossil record. Proc. Geol. Assoc. 87:131-159.

Anderson, T. J. & R. D. Adlard. 1994. Nucleotide sequence of a rDNA internal transcribed spacer supports synonymy of Saccostrea commercialis and S. glomerata. J. Molluscan Stud. 60:196-197.

Bayne, B. 2017. Biology of oysters. London: Academic Press. 860 pp. Bayne, B., M. Ahrens, S. K. Allen, M. Angles d'Auriac, T. Backeljau, P. Beninger, R. Bohn, P. Boudry, J. Davis, T. Green, X. Guo, D. Hedgecock, A. Ibarra, P. Kingsley-Smith, M. Krause, C. Langdon. S. Lapegue, C. Li, D. Manahan. R. Mann, L. Perez-Paralle, E. N. Powell, P. D. Rawson, D. Speiser, J.-L. Sanchez, S. Shumway & H. Wang. 2017. The proposed dropping of the genus Crassostrea for all Pacific cupped oysters and its replacement by a new genus Magallana: a dissenting view. J. Shellfish Res. 36:545-547.

Bayne, B., M. Angles dAuriac, T. Backeljau, P. Beninger, P. Boudry, R. Carnegie, J. Davis, X. Guo, D. Hedgecock, M. Krause, C. Langdon, S. Lapegue, D. Manahan, R. Mann, E. Powell & S. Shumway. 2018. A scientific name for Pacific oysters. Aquaculture (in press), doi: 10.1016/j.aquaculture.2018.08.48.

Beck, M. W., R. D. Brumbaugh, L. Airoldi, A. Carranza, L. D. Coen, C. Crawford, O. Defeo, G. J. Edgar, B. Hancock, M. C. Kay, H. S. Lenihan, M. W. Luckenbach, C. L. Toropova, G. Zhang & X. Guo. 2011. Oyster reefs at risk and recommendations for conservation, restoration, and management. Bioscience 61:107-116.

Bieler, R., P. M. Mikkelsen, T. Lee & D. 6. Foighil. 2004. Discovery of the Indo-Pacific oyster Hyotissa hyolis (Linnaeus, 1758) in the Florida Keys (Bivalvia: Gryphaeidae). Molluscan Res. 24:149-159.

Bouckaert, R., J. Heled, D. Kiihnert, T. Vaughan, C.-H. Wu, D. Xie, M. A. Suchard, A. Rambaut & A. J. Drummond. 2014. BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput. Biol. 10:el003537.

Buroker, N. E. 1983. Population genetics of the American oyster Crassostrea virginica along the Atlantic coast and the Gulf of Mexico. Mar. Biol. 75:99-112.

Buroker, N. E., W. K. Hershberger & K. K. Chew. 1979. Population genetics of the family ostreidae. I. Intraspecific studies of Crassostrea gigas and Saccostrea commercialis. Mar. Biol. 54:157-169.

Calvo, L. M. R., G. W. Calvo & E. M. Burreson. 2003. Dual disease resistance in a selectively bred eastern oyster, Crassostrea virginica, strain tested in Chesapeake Bay. Aquaculture 220:69-87.

Coan, E. V., P. Valentich-Scott & F. R. Bernard. 2000. Bivalve seashells of western North America: marine bivalve mollusks from artic Alaska to Baja California. Santa Barbara Museum of Natural History Monographs 2:1-746.

Coan, E. V. & P. Valentich-Scott. 2012. Bivalve seashells of tropical West America: marine bivalve mollusks from Baja California to northern Peru. Santa Barbara Museum of Natural History Monographs 6:1-1258.

Cordes, J. F., J. Xiao & K. S. Reece. 2008. Discrimination of nine Crassostrea oyster species based upon restriction fragment-length polymorphism analysis of nuclear and mitochondrial DNA markers. J. Shellfish Res. 27:1155-1161.

Darriba, D., G. L. Taboada, R. Doallo & D. Posada. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772.

Dey, A. 2008. Commercial and medicinal important molluscs of sun-darbans. Records of the zoological survey of India. Paper No. 286. West Bengal, India: Zoological Survey of India, pp. 1-54.

do Amaral, V. S. &L. R. L. Simone. 2016. Comparative anatomy of five species of Saccostrea Dollfus and Dautzenberg, 1920 (Bivalvia: Ostreidae) from the Pacific Ocean. Nautilus 130:53-71.

Du, X., G. Fan, Y. Jiao, H. Zhang, X. Guo, R. Huang, Z. Zheng, C. Bian, Y. Deng, Q. Wang, Z. Wang, X. Liang, H. Liang, C. Shi, X. Zhao, F. Sun, R. Hao, J. Bai, J. Liu, W. Chen, J. Liang, W. Liu, Z. Xu, Q. Shi, X. Xu, G. Zhang & X. Liu. 2017. The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization. Gigascience 6:1-12.

Eierman, L. E. & M. P. Hare. 2014. Transcriptomic analysis of candidate osmoregulatory genes in the eastern oyster Crassoslrea virginica. BMC Genomics 15:503.

Erwin, D. H. 1994. The Permo-Triassic extinction. Nature 367:231. Ezkurdia, I., D. Juan, J. M. Rodriguez, A. Frankish, M. Diekhans, J. Harrow, J. Vazquez, A. Valencia & M. L. Tress. 2014. Multiple evidence strands suggest that there may be as few as 19,000 human protein-coding genes. Hum. Mol. Genet. 23:5866-5878.

Fan, C.-F., J.-F. Li, H. Wang, Y.-Z. Yan, F. Wang, Y.-D. Pei & Z.-W. Shang. 2005. Age and paleoenvironmental change of Dawuzhuang oyster reef on the northwest coast of Bohai Bay. Geol. Surv. Res. 28:124-129.

FAO. 2018. Global Aquaculture Production. United Nations Fisheries and Aquaculture Department. Available at: http://www.fao.org/statistics/en/.

Fleury, E., A. Huvet, C. Leiong, J. De Lorgeril, V. Boulo, Y. Gueguen. E. Bachere, A. Tanguy, D. Moraga, C. Fabioux, P. Lindeque, J. Shaw, R. Reinhardt, P. Prunet, G. Davey, S. Lapegue, C. Sauvage, C. Corporeau, J. Moal, F. Gavory, P. Wincker, F. Moreews, C. Klopp, M. Mathieu, P. Boudry & P. Favrel. 2009. Generation and analysis of a 29,745 unique expressed sequence tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics 10:341.

Ford, S. E. & H. H. Haskin. 1987. Infection and mortality patterns in strains of oysters Crassostrea virginica selected for resistance to the parasite Haplosporidium nelsoni (MSX). J. Parasitol. 73:268-376.

Fraiser, M. L. & D. J. Bottjer. 2007. When bivalves took over the world. Paleobiology 33:397-413.

Galtsoff, P.S.I 964. The American oyster, Crassoslrea virginica Gmelin. Fishery Bulletin 64:1-488.

Guo, X. 2009. Use and exchange of genetic resources in molluscan aquaculture. Rev. Aquacult. 1:251-259.

Guo, X. & S. E. Ford. 2016. Infectious diseases of marine molluscs and host responses as revealed by genomic tools. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371:20150206.

Guo, X., Y. He, L. Zhang, C. Leiong & A. Jouaux. 2015. Immune and stress responses in oysters with insights on adaptation. Fish Shellfish Immunol. 46:107-119.

Guo, X., C. Milbury, Y. Wang, Y. He, L. Zhang, D. Bushek & S. Ford. 2012. Genetic structure of eastern oyster populations in Delaware day and selection by diseases. J. Shellfish Res. 31:292.

Guo, X., H. Wang, L. Qian, G. Zhang, X. Liu, F. Xu, X. Wang, T. Okimato, Y. Wang & A. Wang. 2008a. Genetic and ecological structures of oyster estuaries in China and factors affecting success of Crassostrea ariakensis: clues from a reclassification. Final Report of NOAA CBO Award NA04NMF4570424. New Jersey. 24 pp.

Guo, X., Y. Wang, L. Wang & J.-H. Lee. 2008b. Oysters. In: Kocher, T. D. & C. Role, editors. Genome mapping and genomics in fishes and aquatic animals. Berlin, Heidelberg: Springer, pp. 163-175.

Guo, X., Y. Wang, Z. Xu & H. Yang. 2009. Chromosome set manipulation in shellfish. In: Burnell, G. & G. Allan, editors. New technologies in aquaculture: improving production efficiency, quality and environmental management. New York, NY: Woodhead Publishing, pp. 165-195.

Guo, X., G. Zhang, L. Qian, H. Wang, X. Liu & A. Wang. 2006. Oysters and oyster farming in China: a review. J. Shellfish Res. 25:734.

Hallam, A. 1989. The case for sea-level change as a dominant causal factor in mass extinction of marine invertebrates. Philos. Trans. R. Soc. Loud. B Biol. Sci. 325:437-455.

Hamaguchi, M., M. Manabe, N. Kajihara, H. Shimabukuro, Y. Yamada & E. Nishi. 2017. DNA barcoding of flat oyster species reveals the presence of Ostrea stentina Payraudeau, 1826 (Bivalvia: Ostreidae) in Japan. Mar. Biodivers. Rec. 10:4.

Hamaguchi, M., H. Shimabukuro, H. Usuki & M. Hori. 2014. Occurrences of the Indo-West Pacific rock oyster Saccoslrea cucullala in mainland Japan. Mar. Biodivers. Rec. 7: e84.

Hare, M. P. & J. C. Avise. 1996. Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305-2315.

Harper, E. M. & P. Skelton. 1993. The Mesozoic marine revolution and epifaunal bivalves. Scr. Geol. Special Issue 2:127-153.

Harry, H. W. 1985. Synopsis of the supraspecific classification of living oysters (Bivalvia: Gryphaeidae and Ostreidae). Vetiger 28:121-158.

Harzhauser, M., A. Djuricic, O. Mandic, T. A. Neubauer, M. Zuschin & N. Pfeifer. 2016. Age structure, carbonate production and shell loss rate in an Early Miocene reef of the giant oyster Crassostrea gry-phoides. Biogeosciences 13:1223-1235.

Hautmann, M.,D. Ware&H. Bucher. 2017. Geologically oldest oysters were epizoans on Early Triassic ammonoids. J. Molluscan Stud. 83:253-260.

Hayami, I. & T. Kase. 1992. 935. A new cryptic species of Pycnodonte from Ryukyu Islands: a living fossil oyster. Transactions and proceedings of the Paleontological Society of Japan, New Series. 1992: 1070-1089.

He, Y., A. Jouaux, S. E. Ford, C. Leiong, P. Sourdaine, M. Mathieu & X. Guo. 2015. Transcriptome analysis reveals strong and complex antiviral response in a mollusc. Fish Shellfish Immunol. 46:131-144.

Hebert, P. D., S. Ratnasingham & J. R. de Waard. 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. B Biol. Sci. 270:S96-S99.

Hedgecock, D. 1994. Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont, A. R, editor. Genetics and evolution of aquatic organisms. London: Chapman & Hall. pp. 122-134.

Hedgecock, D., P. Gaffney, P. Goulletquer, X. Guo, K. Reece & G. Warr. 2005. The case for sequencing the Pacific oyster genome. J. Shellfish Res. 24:429-441.

Hinegardner, R. 1974. Cellular DNA content of the mollusca. Comp. Biochem. Physiol. 47A:447-460.

Hofmann, E., D. Bushek, S. Ford, X. Guo. D. Haidvogel, D. Hedgecock, J. Klinck, C. Milbury, D. Narvaez, E. Powell, Y. Wang, Z. Wang, J. Wilkin & L. Zhang. 2009. Understanding how disease and environment combine to structure resistance in estuarine bivalve populations. Oceanography 22:212-231.

Hong, W., E. Keppens, P. Nielsen & A. van Riet. 1995. Oxygen and carbon isotope study of the Holocene oyster reefs and paleoenvironmental reconstruction on the northwest coast of Bohai Bay, China. Mar. Geol. 124:289-302.

Huber, M. 2010. Compendium of bivalves. A full-color guide to 3,300 of the world's marine bivalves. A status on bivalvia after 250 years of research. Hackenheim, Germany: ConchBooks. 901 pp.

Huber. M., A. Langleit & K. Kreipl. 2015. Compendium of bivalves 2. Hackenheim, Germany: ConchBooks. 907 pp.

Huber, M. & F. Lorenz. 2007. Empressostrea kostini n. gen., n. sp. (Bivalvia: Ostreoidea), a mysterious giant oyster from the Spratly Islands, South China Sea. Club Conchylia Informalionen 38:26-41.

Hurwood, D. A., M. P. Heasman & P. B. Mather. 2005. Gene flow, colonisation and demographic history of the flat oyster Ostrea angasi. Mar. Freshwater Res. 56:1099-1106.

Huvet, A., C. Fabioux, H. McCombie, S. Lapegue & P. Boudry. 2004. Natural hybridization between genetically differentiated populations of Crassostrea gigas and C. angulata highlighted by sequence variation in flanking regions of a microsatellite locus. Mar. Ecol. Prog. Ser. 272:141-152.

Jia, Y. & D. Tian. 1996. Ocean and land processes in ancient Bohai Sea. J. Tianjin Normal Univ. 16:42-46 (Natural science edition).

Jozefowicz, C. J. & D. O. Foighil. 1998. Phylogenetic analysis of southern hemisphere flat oysters based on partial mitochondrial 16S rDNA gene sequences. Mol. Phylogenet. Evol. 10:426-435.

Karl, S. A. & J. C. Avise. 1992. Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256: 100-102.

Kenchington, E., C. J. Bird, J. Osborne & M. Reith. 2002. Novel repeat elements in the nuclear ribosomal RNA operon of the flat oysters Ostrea edulis Linnaeus, 1758 and O. angasi Sowerby, 1871. J. Shellfish Res. 21:697-705.

Kirkendale, L., T. Lee, P. Baker & D. 6. Foighil. 2004. Oysters of the Conch Republic (Florida Keys): a molecular phylogenetic study of Parahyolissa mcgintyi, Teskeyostrea weberi and Ostreola equestris. Malacologia 46:309-326.

Klinbunga, S., B. Khamnamtong, N. Puanglarp, P. Jarayabhand, W. Yoosukh & P. Menasverta. 2005. Molecular taxonomy of cupped oysters (Crassostrea, Saccostrea, and Striostrea) in Thailand based on COI, 16S, and 18S rDNA polymorphism. Mar. Biotechnol. 7:306-317.

Klinbunga, S., N. Khamnamtong, A. Tassanakajon, N. Pauanglarp, P. Jarayahand & W. Yoosukh. 2003. Molecular genetic identification tools for three commercially cultured oysters (Crassostrea belcheri, Crassostrea iredalei, and Saccostrea cucullata) in Thailand. Mar. Biotechnol. 5:27-36.

Kumar, S., G. Stecher & K. Tamura. 2016. MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870.

Lam, K. & B. Morton. 2003. Mitochondrial DNA and morphological identification of a new species of Crassostrea (Bivalvia: Ostreidae) cultured for centuries in the Pearl River Delta, Hong Kong, China. Aquaculture 228:1-13.

Lam, K. & B. Morton. 2006. Morphological and mitochondrial-DNA analysis of the Indo-West Pacific rock oysters (Ostreidae: Saccostrea species). J. Molluscan Stud. 72:235-245.

Lambeck, K., T. M. Esat & E.-K. Potter. 2002. Links between climate and sea levels for the past three million years. Nature 419:199.

Lapegue, S., F. Batista, S. Heurtebise, Z. Yu & P. Boudry. 2004. Evidence for the presence of the Portuguese oyster, Crassostrea angulata, in northern China. J. Shellfish Res. 23:759-763.

Lapegue, S., I. Boutet, A. Leitao, S. Heurtebise, P. Garcia, C. Thiriotquievreux & P. Boudry. 2002. Trans-Atlantic distribution of a mangrove oyster species revealed by 16S mtDNA and karyological analysis. Biol. Bull. 202:232-242.

Lapegue, S., I. B. Salah, F. M. Batista, S. Heurtebise, L. Neifar & P. Boudry. 2006. Phylogeographic study of the dwarf oyster, Ostreola slentina, from Morocco, Portugal and Tunisia: evidence of a geographic disjunction with the closely related taxa, Ostrea aupouria and Ostreola equestris. Mar. Biol. 150:103-110.

Launey, S. & D. Hedgecock. 2001. High genetic load in the pacific oyster Crassostrea gigas. Genetics 159:255-265.

Lazoski, C, J. Gusmao, P. Boudry & A. Sole-Cava. 2011. Phylogeny and phylogeography of Atlantic oyster species: evolutionary history, limited genetic connectivity and isolation by distance. Mar. Ecol. Prog. Ser. 426:197-212.

Li, C. 2013. Phylogeny and evolutionary analysis of oysters (Bivalvia: Ostreoidea) and complete mitochondrial DNA of Talonostrea talonata. M.S. Thesis. Qingdao, China: University of Chinese Academy of Sciences. 56 pp.

Li, C, M. Haws, H. Wang & X. Guo. 2017b. Taxonomic classification of three oyster (Ostreidae) species from Myanmar. J. Shellfish Res. 36:365-371.

Li, C, H. Wang & X. Guo. 2017a. Classification and taxonomic revision of two oyster species from Peru: Ostrea megodon (Hanley, 1846) and Crassostrea talonata (Li & Qi, 1994). J. Shellfish Res. 36:359-364.

Li, L., A. Li, K. Song, J. Meng, X. Guo, S. Li, C. Li, P. D. Wit, H. Que, F. Wu, W. Wang, H. Qi, F. Xu, R. Cong, B. Huang, Y. Li, T. Wang, X. Tang, S. Liu, B. Li, R. Shi, Y. Liu. C. Bu, C. Zhang, W. He. S. Zhao, H. Li, S. Zhang, L. Zhang &G. Zhang. 2018. Divergence and plasticity shape adaptive potential in the Pacific oyster. Nat. Ecol. Evol. (in press). DOI: 10.1038/s41559-018-0668-2.

Li, L. & X. Guo. 2004. AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas Thunberg. Mar. Biotechnol. 6:26-36.

Li, X. & Z. Qi. 1994. Studies on the comparative anatomy, systematic classification and evolution of Chinese oysters. Stud. Mar. Sin. 35:143-173.

Li, Y., X. Sun, X. Hu, X. Xun, J. Zhang. X. Guo, W. Jiao, L. Zhang, W. Liu, J. Wang, J. Li, Y. Sun, Y. Miao, X. Zhang, T. Cheng, G. Xu, X. Fu, Y. Wang, X. Yu, X. Huang, W. Lu, J. Lv, C. Mu, D. Wang, X. Li, Y. Xia, Y. Li, Z. Yang, F. Wang, L. Zhang, Q. Xing, H. Dou, X. Ning, J. Dou, Y. Li, D. Kong, Y. Liu, Z. Jiang, R. Li, S. Wang & Z. Bao. 2017c. Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins. Nat. Commun. 8:1721.

Linnaeus, C. 1758. Systema naturae, 10 (th) edition, vol. 1. Stockholm, Sweden: L. Salvii. 824 pp.

Liu, J., Q. Li, L. Kong, H. Yu & X. Zheng. 2011. Identifying the true oysters (Bivalvia: Ostreidae) with mitochondrial phylogeny and distance-based DNA barcoding. Mol. Ecol. Resour. 11:820-830.

Liu, Y., H. Huang, Y. Qi, X. Liu & X. Yang. 2016. Holocene coastal morphologies and shoreline reconstruction for the southwestern coast of the Bohai Sea, China. Quat. Res. 86:144-161.

Marquez-Aliaga, A., A. P. Jimenez-Jimenez, A. G. Checa & H. Hagdorn. 2005. Early oysters and their supposed Permian ancestors. Palaeogeogr. Palaeoclimatol. Palaeoecol. 229:127-136.

McDonnell Genome Institute, Washington University School of Medicine. 2017. C_virginica-3.0. National Center for Biotechnology Information, U.S. National Library of Medicine online database.

Menzel, R. W. 1974. Portuguese and Japanese oysters are the same species. J. Fish. Res. Board Can. 31:453-455.

Miller, K. G., M. A. Kominz, J. V. Browning, J. D. Wright, G. S. Mountain, M. E. Katz, P. J. Sugarman, B. S. Cramer, N. Christie-Blick & S. F. Pekar. 2005. The Phanerozoic record of global sea-level change. Science 310:1293-1298.

MolluscaBase. 2018a. Ostrea atherstonei Newton, 1913. Accessed September 11, 2018. World Register of Marine Species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=224651.

MolluscaBase. 2018b. Pustulostrea australis (Lamarck, 1819). Accessed September 11, 2018. World Register of Marine Species at: http://marinespecies.org/aphia.php?p=taxdetails&id=506727.

Mou, C. & C. Liu. 1993. Permian bivalves from the area of Guangzhou. Acta Sci. Natur. Univ. Sunyatseni 32:101-108.

Nakazawa, K. & D. N. Newell. 1968. Permian bivalves of Japan. Memoirs of the Faculty of Science, Kyoto University. Series of Geology and Mineralogy 35:1-108.

Foighil, D. O. & D. J. Taylor. 2000. Evolution of parental care and ovulation behavior in oysters. Mol. Phylogenet. Evol. 15:301-313.

Palumbi, S. R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Syst. 25:547-572.

Plough, L. V. 2016. Genetic load in marine animals: a review. Current Zoology 62:567-579.

Poison, M. P., W. E. Hewson, D. J. Eernisse, P. K. Baker & D. C. Zacherl. 2009. You say conchaphila, I say lurida: molecular evidence for restricting the Olympia oyster (Ostrea lurida Carpenter 1864) to temperate western North America. J. Shellfish Res. 28:11-21.

Raith, M., D. C. Zacherl, E. M. Pilgrim & D. J. Eernisse. 2016. Phylogeny and species diversity of Gulf of California oysters (Ostreidae) inferred from mitochondrial DNA. Am. Malacol. Bull. 33:263-283.

Reece, K. S., J. F. Cordes. J. B. Stubbs, K. L. Hudson & E. A. Francis. 2008. Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Mar. Biol. 153:709-721.

Ren, J., Z. Hou, H. Wang, M.-A. Sun, X. Liu. B. Liu & X. Guo. 2016. Intraspecific variation in mitogenomes of five Crassostrea species provides insight into oyster diversification and speciation. Mar. Biotechnol. (NY) 18:242-254.

Ren, J., X. Liu, F. Jiang, X. Guo & B. Liu. 2010. Unusual conservation of mitochondrial gene order in Crassostrea oysters: evidence for recent speciation in Asia. BMC Evol. Biol. 10:394.

Salvi, D., A. Macali & P. Mariottini. 2014. Molecular phylogenetics and systematics of the bivalve family Ostreidae based on rRNA sequence-structure models and multilocus species tree. PLoS One 9:el08696.

Salvi, D. & P. Mariottini. 2017. Molecular taxonomy in 2D: a novel ITS2 rRNA sequence-structure approach guides the description of the oysters' subfamily Saccostreinae and the genus Magallana (Bivalvia: Ostreidae). Zool. J. Linn. Soc. 179:263-276.

Schulte, P.. L. Alegret, I. Arenillas, J. A. Arz, P. J. Barton, P. R. Bown, T. J. Bralower, G. L. Christeson, P. Claeys & C. S. Cockell. 2010. The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327:1214-1218.

Sekino, M. & H. Yamashita. 2016. Mitochondrial and nuclear DNA analyses of Saccostrea oysters in Japan highlight the confused taxonomy of the genus. J. Molluscan Stud. 82:492-506.

Shilts, M. H., M. S. Pascual & D. 6. Foighil. 2007. Systematic, taxonomic and biogeographic relationships of Argentine flat oysters. Mol. Phylogenet. Evol. 1:467-473.

Stenzel, H. B. 1971. Oysters. In: Moore, R. C, editor. Treatise Invertebrate Paleont., Part N, Bivalvia 3. Lawrence, KS: Geological Society of America and University of Kansas, pp. N953-N1224. N953-1224.

Sun, J., Y. Zhang, T. Xu, Y. Zhang, H. Mu, Y. Zhang, Y. Lan, C. J. Fields, J. H. L. Hui, W. Zhang, R. Li, W. Nong, F. K. M. Cheung, J.-W. Qiu & P.-Y. Qian. 2017. Adaptation to deep-sea chemosyn-thetic environments as revealed by mussel genomes. Nat. Ecol. Evol. 1:0121.

Torigoe, K. 1981. Oysters in Japan. J. Sci. Hiroshima Univ. Ser. B. Div. 1291-481.

Vermeij, G. J. 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3:245-258.

Wang, H. & X. Guo. 2008a. Identification of Crassostrea ariakensis and related oysters by multiplex species-specific PCR. J. Shellfish Res. 27:481-487.

Wang, H., X. Guo. G. Zhang & F. Zhang. 2004a. Classification of jinjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquacullure 242:137-155.

Wang, H., L. Qian, X. Liu, G. Zhang & X. Guo. 2010. Classification of a common cupped oyster from Southern China. J. Shellfish Res. 29:857-866.

Wang, PL, L. Qian, A. Wang & X. Guo. 2013. Occurrence and distribution of Crassostrea sikamea (Amemiya, 1928) in China. J. Shellfish Res. 32:439^146.

Wang, S., J. Zhang, W. Jiao, J. Li, X. Xun, Y. Sun, X. Guo, P. Huan, B. Dong, L. Zhang, X. Hu, X. Sun, J. Wang, C. Zhao, Y. Wang, D. Wang, X. Huang, R. Wang, J. Lv, Y. Li, Z. Zhang, B. Liu, W. Lu, Y. Hui, J. Liang, Z. Zhou, R. Hou, X. Li, Y. Liu, H. Li, X. Ning, Y. Lin, L. Zhao, Q. Xing, J. Dou, Y. Li, J. Mao, H. Guo, H. Dou, T. Li, C. Mu, W. Jiang, Q. Fu, X. Fu, Y. Miao. J. Liu. Q. Yu, R. Li, H. Liao, X. Li, Y. Kong, Z. Jiang, D. Chourrout, R. Li & Z. Bao. 2017b. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat. Ecol. Evol. 1:0120.

Wang, X., L. Kong, J. Chen, A. Matsukuma & Q. Li. 2017a. Phylogeography of bivalve Meretrix peteehialis in the northwestern Pacific indicated by mitochondrial and nuclear DNA data. PLoS One 12:e0183221.

Wang, Y. & X. Guo. 2004. Chromosomal rearrangement in pectinidae revealed by rRNA loci and implications for bivalve evolution. Biol. Bull. 207:247-256.

Wang, Y. & X. Guo. 2008b. Its length polymorphism in oysters and its use in species identification. J. Shellfish Res. 27:489-193.

Wang, Y.. Z. Xu & X. Guo. 2004b. Differences in the rDNA-bearing chromosome divide the Asian-Pacific and Atlantic species of Crassostrea (Bivalvia, Mollusca). Biol. Bull. 206:46-54.

Wignall, P. & A. Hallam. 1992. Anoxia as a cause of the Permian/Triassic mass extinction: fades evidence from northern Italy and the western United States. Palaeogeogr. Palaeoclimatol. Palaeoecol. 93:21-46.

Wilke, T., R. SchultheiB & C. Albrecht. 2009. As time goes by: a simple fool's guide to molecular clock approaches in invertebrates. Am. Malacoi. Bull. 27:25-15.

Wisshak, M., M. L. Correa, S. Gofas, C. Salas, M. Taviani, J. Jakobsen & A. Freiwald. 2009. Shell architecture, element composition, and stable isotope signature of the giant deep-sea oyster Neopycnodonte zibrowii sp. n. from the NE Atlantic. Deep Sea Res. Part I Oceanogr. Res. Pap. 56:374-407.

Wu. X., S. Xiao & Z. Yu. 2013. Mitochondrial DNA and morphological identification of Crassostrea ihanjiangensis sp. nov. (Bivalvia: Ostreidae): a new species in Zhanjiang, China. Aquat. Living Resour. 26:273-280.

Xia, J., X. Wu, S. Xiao & Z. Yu. 2014. Mitochondrial DNA and morphological identification of a new cupped oyster species Crassostrea dianbaiensis (Bivalvia: Ostreidae) in the South China Sea. Aquat. Living Resour. 27:41-48.

Xu, F. 1997. Bivalve molluscan of China. Beijing, China: Science Press. 333 pp.

Zhang, G., X. Fang, X. Guo, L. Li, R. Luo, F. Xu, P. Yang, L. Zhang, X. Wang, H. Qi, Z. Xiong, H. Que, Y. Xie, P. W. H. Holland, J. Paps, Y. Zhu, F. Wu, Y. Chen, J. Wang, C. Peng, J. Meng, L. Yang, J. Liu, B. Wen, N. Zhang, Z. Huang, Q. Zhu, Y. Feng, A. Mount, D. Hedgecock, Z. Xu, Y. Liu, T. Domazet-Loso, Y. Du, X. Sun, S. Zhang, B. Liu, P. Cheng, X. Jiang, J. Li. D. Fan, W. Wang. W. Fu, T. Wang, B. Wang, J. Zhang, Z. Peng, Y. Li, N. Li, J. Wang, M. Chen, Y. He, F. Tan, X. Song, Q. Zheng, R. Huang, H. Yang, X. Du, L. Chen, M. Yang, P. M. Gaffney, S. Wang, L. Luo, Z. She, Y. Ming, W. Huang, S. Zhang, B. Huang, Y. Zhang, T. Qu, P. Ni, G. Miao, J. Wang, Q. Wang, C. E. W. Steinberg, H. Wang, N. Li, L. Qian, G. Zhang, Y. Li, H. Yang, X. Liu, J. Wang, Y. Yin & J. Wang. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49-54.

Zhang, L. & X. Guo. 2010. Development and validation of single nucleotide polymorphism markers in the eastern oyster Crassostrea virginica Gmelin by mining ESTs and resequencing. Aquacullure 302:124-129.

Zhang, L., L. Li, X. Guo, G. W. Litman, L. J. Dishaw & G. Zhang. 2015. Massive expansion and functional divergence of innate immune genes in a protostome. Sci. Rep. 5:8693.

Zhang, L., L. Li, Y. Zhu, G. Zhang & X. Guo. 2014. Transcriptome analysis reveals a rich gene set related to innate immunity in the eastern oyster (Crassostrea virginica). Mar. Biotechnol. (NY) 16:17-33.

Zhang, X. & Z. Lou. 1956. Studies on oysters in China. Dong Wu Xue Bao 8:65-94.

XIMING GUO, (1*) CUI LI, (1,2,3) HAIYAN WANG (2,3) AND ZHE XU (4)

(1) Haskin Shellfish Research Laboratory, Department of Marine and Coastal Sciences, Rutgers University, 6959 Miller Avenue, Port Norris, NJ08349; (2) Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, Shandong 266071, China; (3) Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, China; (4) Science Department, Atlantic Cape Community College, 5100 Black Horse Pike, Mays Landing, New Jersey 08330

(*) Corresponding author. E-mail: xguo@hsrl.rutgers.edu

DOI: 10.2983/035.037.0407
TABLE 1.
Higher level classification of living oysters by different authors.

Family               Subfamily

Stenzel (1971)
Gryphaeidae          Pycnodonteinae
Ostreidae            Lophinae
                     Ostreinae
Torigoe(1981)
Pycnodonteidae (*)
Ostreidae            Crassostreinae (*)
                     Lophinae
                     Ostreinae
Harry (1985)
Gryphaeidae          Pycnodonteinae
Ostreidae            Crassostreinae
                     Lophinae

                     Ostreinae


Li and Qi(1994)
Gryphaeidae          Pycnodonteinae
Ostreidae            Crassostreinae
                     Lophinae
                     Ostreinae
Li(2013)
Gryphaeidae          Pycnodonteinae
Ostreidae            Crassostreinae
                     Ostreinae

                     Saccostreinae (*)
Salvi et al. (2014)
Gryphaeidae
Ostreidae            Crassostreinae
                     Ostreinae
                     Saccostreinae
Raith et al. (2016)
Ostreidae            Crassostreinae
                     Ostreinae
                     Saccostreinae
                     Striostreinae (*)
This study
Gryphaeidae          Pycnodonteinae
Ostreidae            Crassostreinae
                     Lophinae
                     Ostreinae

                     Saccostreinae
                     Striostreinae

Family               Genus

Stenzel (1971)
Gryphaeidae          Hyotissa, Neopycnodonte
Ostreidae            Alectryonella, Lopha
                     Crassostrea, Ostrea, Saccostrea, Striostrea
Torigoe(1981)
Pycnodonteidae (*)   Hyolissa, Neopycnodonte
Ostreidae            Crassostrea, Saccostrea
                     Alectryonella, Dendostrea, Lopha
                     Ostrea
Harry (1985)
Gryphaeidae          Hyotissa, Neopycnodonte, Parahyotissa (*)
Ostreidae            Crassostrea, Saccostrea, Striostrea
                     Alectryonella, Anomiostrea, Dendostrea, Lopha,
                     Myrakeena (*)
                     Booneostrea (*), Cryptostrea (*), Nanostrea (*),
                     Ostrea,
                     Ostreola, Planostrea (*), Pustulostrea (*),
                     Teskeyostrea (*),
                     Undulostrea (*)
Li and Qi(1994)
Gryphaeidae          Hyotissa, Neopycnodonte
Ostreidae            Crassostrea, Saccostrea, Talonostrea (*)
                     Alectryonella, Dendostrea, Lopha
                     Ostrea, Planostrea
Li(2013)
Gryphaeidae          Hyotissa, Neopycnodonte
Ostreidae            Crassostrea, Talonostrea
                     Alectryonella, Dendostrea, Lopha, Ostrea,
                     Planostrea,
                     Teskeyostrea
                     Saccostrea
Salvi et al. (2014)
Gryphaeidae          Hyolissa, Neopycnodonte
Ostreidae            Crassostrea, Magallana (*), Talonostrea
                     Alectryonella, Cryptostrea, Dendostrea, Lopha,
                     Ostrea
                     Saccostrea
Raith et al. (2016)
Ostreidae            Crassostrea
                     Alectryonella, Dendostrea, Lopha, Ostrea
                     Saccostrea
                     Striostrea
This study
Gryphaeidae          Hyotissa, Neopycnodonte, Pycnodonte, Empressostrea
Ostreidae            Crassostrea
                     Alectryonella, Dendostrea, Lopha, Nicaisolopha
                     Anomiostrea, Ostrea, Booneostrea, Planostrea,
                     Pustulostrea
                     Saccostrea
                     Striostrea

(*)Designates new taxa proposed.

TABLE 2.
Kimura 2-parameter genetic distances in mitochondrial COI gene within
and between selected oyster species.

Species/Species Pair                     COI(%)

Crassostrea gigas                         0.2-0.9
Crassostrea angnlita                      0.7-1.5
Crassostrea virginica                     0.6-2.2
Crassostrea ariakensis                    0.2-1.0
Crassostrea iredalei                      0.2-3.3
Crassostrea talonata: China (n = 12)      0.2-3.7
Ostrea angasi (n = 31)                    0.3-1.0
Ostrea edulis (n = 7)                     0.3-1.6
Ostrea permollis: USA (n; = 9)            0.5-2.4
Ostrea puekhana: Argentina (n = 4)        0.5-2.0
C. gigas vs. angulata                     2.2-3.6
C. talonata: China vs. Peru               3.6
Crassostera gryphoides dwarkaensis vs.
tanintharyiensis                          2.8-3.2
Ostrea conchaphila vs. lurida (n = 70)    3.6-4.7
0. edulis vs. angasi (n = 38)             1.3-2.9
0. permollis vs. puekhana (n = 13)        2.2-3.8
Ostrea stenlina complex (n = 15)          0.2-5.4
Saceostrea mordax complex (n = 7)         0.3-10.1
C. gigas vs. C. sikamea                   9.92-10.3
C. gigas vs. virginica                   25.6-27.2
C. virginica vs. columbiensis            28.9

Species/Species Pair                     Reference

Crassostrea gigas                        Wang et al. (2010)
Crassostrea angnlita                     Wang et al. (2010)
Crassostrea virginica                    Wang et al. (2010)
Crassostrea ariakensis                   Wang et al. (2004a)
Crassostrea iredalei                     This study (*)
Crassostrea talonata: China (n = 12)     This study
Ostrea angasi (n = 31)                   This study
Ostrea edulis (n = 7)                    This study
Ostrea permollis: USA (n; = 9)           This study
Ostrea puekhana: Argentina (n = 4)       This study
C. gigas vs. angulata                    Wang et al. (2010)
C. talonata: China vs. Peru              Li et al. (2017a)
Crassostera gryphoides dwarkaensis vs.
tanintharyiensis                         Li et al. (2017b)
Ostrea conchaphila vs. lurida (n = 70)   This study
0. edulis vs. angasi (n = 38)            This study
0. permollis vs. puekhana (n = 13)       This study
Ostrea stenlina complex (n = 15)         This study: 3 species
Saceostrea mordax complex (n = 7)        This study: 2-3 species
C. gigas vs. C. sikamea                  Wang et al. (2010)
C. gigas vs. virginica                   Wang et al. (2010)
C. virginica vs. columbiensis            Li et al. (2017a)

TABLE 3.
A list of living oyster species and their geographic distribution, den
Bank accession numbers are provided when available for COI
(mitochondrial cytochrome c oxidase subunit I) and 16S (mitochondrial
16S ribosomal RNA) fragments.

Species                                                   COI

Pycnodonteinae
Empressostrea koslini (Huber & Lorenz 2007)
Hyotissa hyotis (Linnaeus 1758)                           GQ166583

Hyotissa fischeri (Dall, 1914)
Hyotissa imbrkata (Lamarck, 1819)                         AB076917
Hyotissa inermis (Sowerby II, 1871)
Hyotissa megintyi (Harry 1985)
Hyotissa numisma (Lamarck, 1819)
Hyotissa quercina (Sowerby II, 1871)
Hyotissa sinensis (Gmelin, 1791)

Neopycnodonte cochlear (Poli, 1795)                       JF496772
Neopycnodonte zibrowii (Gofas, Salas & Taviani, 2009)

Pycnodonte taniguchii (Hayami & Kase 1992)                AB076916

Crassostreinae
Crassostrea aequalorialis (d'Orbigny, 1846)
Crassostrea angulata (Lamarck, 1819)                      KP216803
Crassostrea ariakensis (Fujita, 1913)                     KF272859

Crassostrea belcheri (G. B. Sowerby II, 1871)             AY 160755

Crassostrea bilineata (Roding, 1798)
Crassostrea brasiliana (Lamarck, 1819)                    FJ717651
Crassostrea columbiensis (Hanley, 1846)                   KP455055
Crassostrea corteziensis (Hertlein, 1951)
Crassostrea cultackensis (Newton & Smith, 1912)

Crassostrea dactylena (Iredale, 1939)
Crassostrea dianbaiensis (Xia et al. 2014)                LC063808
Crassostrea gryphoides dwarkaensis (Reece et al. 2008)    EU007492
Crassostrea gigas (Thunberg, 1793)                        KP099052
Crassostrea hongkongensis (Lam & Morton 2003)             KP976208
Crassostrea iredalei (Faustino, 1932)                     KU947196

Crassostrea madrasensis (Preston, 1916)                   GU591435

Crassostrea mangle (Amaral & Simone, 2014)
Crassostrea nippona (Seki, 1934)                          LC005437
Crassostrea praia (Ihering, 1907)
Crassostrea rhizophorae (Guilding, 1828)                  KP455050
Crassostrea sikamea (Amemiya, 1928)                       AB904878
Crassostrea talonata (Li & Qi 1994) China                 KC683515
Crassostrea talonata (Li & Qi 1994) Peru                  KX364277
Crassostrea gryphoides tanintharyiensis (Li et al. 2017)  KX961667
Crassostrea titlipa (Lamarck, 1819)
Crassostrea virginica (Gmelin, 1791)                      KF644145
Crassostrea zhanjiangensis (Wu et al. 2013)               JX899646
Lophinae
Alectryonella plicatula (Gmelin, 1791)
Lopha cristagalli (Linnaeus 1758)                         AB076908
Dendostrea erenulifera (G. B. Sowerby II, 1871)           KC683510
Dendostrea cristata (Born, 1778)
Dendostrea folium (Linnaeus 1758)
Dendostrea from (Linnaeus 1758)                           KP455014
Dendostrea rosacea (Deshayes, 1836)
Dendostrea sandxichensis (G. B. Sowerby II, 1871)
Dendostrea senegalensis (Gmelin, 1791)
Dendostrea trapezina (Lamarck, 1819)
Nicaisolopha tridacnaeformis (Cox, 1927)
Ostreinae
Anomiostrea coralliophila (Habe, 1975)
Booneostrea subucula (Jousseaume in Lamy, 1925)           LC149516

Ostrea fluctigera (Jousseaume in Lamy, 1925)              LC149507
Ostrea algoensis (Sowerby 11, 1871)
Ostrea angasi (G. B. Sowerby II, 1871)                    AF112287
Ostrea angelica (Rochebrune, 1895)                        KT317451
Ostrea atherstonei (Newton, 1913)
Ostrea circumpicta (Pilsbry, 1904)                        AB898294
Ostrea chilensis (Philippi, 1844)                         AF112289
Ostrea conchaphila (Carpenter, 1857)                      KT317465
Ostrea denselamellosa (Lischke, 1869)                     KP067908
Ostrea edulis (Linnaeus 1758)                             KJ818235

Ostrea futamiensis (Seki, 1929)                           LC051627
Ostrea libella (Weisbord, 1964)
Ostrea lurida (Carpenter, 1864)                           KT317519
Ostrea megodon (Hanley, 1846)                             KX364276
Ostrea permollis (G. B. Sowerby II, 1871)                 DQ226524
Ostrea puelchana (d'Orbigny, 1842)                        DQ226518
Ostrea equestris (Say, 1834)                              KT317503

Ostrea stentina (Payraudeau, 1826) A                      DQ313182

Ostrea stentina (Payraudeau, 1826) B                      DQ313181

Ostrea weberi (Olsson, 1951)
Planostrea pestigris (Hanley, 1846)
Pustulostrea australis (Lamarck, 1819)
Pustulostrea pseudangulata (Lamy, 1930)
Saccostreinae
Saccostrea circumsuta (Gould, 1850)
Saccostrea cucullata (Born, 1778) A

Saccostrea cucullata (Born, 1778) B

Saccostrea cucullata (Born, 1778) C                       LCI 10533
Saccostrea cucullata (Born, 1778) D
Saccostrea cucullata (Born, 1778) E
Saccostrea cucullata (Born, 1778) G                       LCI 10526
Saccostrea cucullata (Born, 1778) H                       LCI 10615
Saccostrea cucullata (Born, 1778) I                       LCI 10579
Saccostrea echinata (Quoy & Gaimard, 1835)                KC683512
Saccostrea glomerata (Gould, 1850)                        LC005435
Saccostrea kegaki (Torigoe & Inaba, 1981)                 LCI 10631
Saccostrea malabonensls (Faustino, 1932)                  LC005431

Saccostrea mordax (Gould, 1850) A                         EU816072
S.mordax (Gould, 1850) B                                  EU816072
S. mordax (Gould, 1850) C                                 AB748841
Saccostrea mytiloides (Lamarck, 1819)                     NC_036479
Saccostrea palmula (Carpenter, 1857)                      KT317530

Saccostrea scyphophilla (Peron & Lesueur, 1807)
Saccostrea spathulata (Lamarck, 1819)
Saccostrea suhtrigona (G. B. Sowerby II, 1871)
Striostreinae
Striostrea demiculata (Born, 1778)
Striostrea margaritacea (Lamarck, 1819)                   LT220875
Striostrea prismatica (Gray, 1825)                        KT317606

Species                                                   16S

Pycnodonteinae
Empressostrea koslini (Huber & Lorenz 2007)
Hyotissa hyotis (Linnaeus 1758)                           AY376599

Hyotissa fischeri (Dall, 1914)
Hyotissa imbrkata (Lamarck, 1819)                         KC847136
Hyotissa inermis (Sowerby II, 1871)
Hyotissa megintyi (Harry 1985)                            AY376597
Hyotissa numisma (Lamarck, 1819)                          AY376598
Hyotissa quercina (Sowerby II, 1871)
Hyotissa sinensis (Gmelin, 1791)                          EU815986

Neopycnodonte cochlear (Poli, 1795)                       JF496758
Neopycnodonte zibrowii (Gofas, Salas & Taviani, 2009)

Pycnodonte taniguchii (Hayami & Kase 1992)

Crassostreinae
Crassostrea aequalorialis (d'Orbigny, 1846)
Crassostrea angulata (Lamarck, 1819)                      KC847117
Crassostrea ariakensis (Fujita, 1913)                     FJ743507

Crassostrea belcheri (G. B. Sowerby II, 1871)             AY160758

Crassostrea bilineata (Roding, 1798)
Crassostrea brasiliana (Lamarck, 1819)                    DQ839413
Crassostrea columbiensis (Hanley, 1846)
Crassostrea corteziensis (Hertlein, 1951)                 KT317088
Crassostrea cultackensis (Newton & Smith, 1912)

Crassostrea dactylena (Iredale, 1939)
Crassostrea dianbaiensis (Xia et al. 2014)                AB972006
Crassostrea gryphoides dwarkaensis (Reece et al. 2008)
Crassostrea gigas (Thunberg, 1793)                        AF280611
Crassostrea hongkongensis (Lam & Morton 2003)             KC847120
Crassostrea iredalei (Faustino, 1932)                     KU947124

Crassostrea madrasensis (Preston, 1916)                   JF915518

Crassostrea mangle (Amaral & Simone, 2014)
Crassostrea nippona (Seki, 1934)                          LC005446
Crassostrea praia (Ihering, 1907)
Crassostrea rhizophorae (Guilding, 1828)                  JN849107
Crassostrea sikamea (Amemiya, 1928)                       KC847116
Crassostrea talonata (Li & Qi 1994) China                 KC847133
Crassostrea talonata (Li & Qi 1994) Peru                  KX364275
Crassostrea gryphoides tanintharyiensis (Li et al. 2017)  KX961681
Crassostrea titlipa (Lamarck, 1819)
Crassostrea virginica (Gmelin, 1791)                      KC429253
Crassostrea zhanjiangensis (Wu et al. 2013)               JX899653
Lophinae
Alectryonella plicatula (Gmelin, 1791)                    AF052072
Lopha cristagalli (Linnaeus 1758)                         AF052066
Dendostrea erenulifera (G. B. Sowerby II, 1871)           KC847121
Dendostrea cristata (Born, 1778)
Dendostrea folium (Linnaeus 1758)                         AF052069
Dendostrea from (Linnaeus 1758)                           AF052070
Dendostrea rosacea (Deshayes, 1836)                       EF122381
Dendostrea sandxichensis (G. B. Sowerby II, 1871)
Dendostrea senegalensis (Gmelin, 1791)
Dendostrea trapezina (Lamarck, 1819)
Nicaisolopha tridacnaeformis (Cox, 1927)
Ostreinae
Anomiostrea coralliophila (Habe, 1975)
Booneostrea subucula (Jousseaume in Lamy, 1925)           LC149513

Ostrea fluctigera (Jousseaume in Lamy, 1925)              LC149503
Ostrea algoensis (Sowerby 11, 1871)                       AF052062
Ostrea angasi (G. B. Sowerby II, 1871)                    AF052063
Ostrea angelica (Rochebrune, 1895)                        KT317142
Ostrea atherstonei (Newton, 1913)
Ostrea circumpicta (Pilsbry, 1904)                        AB898282
Ostrea chilensis (Philippi, 1844)                         AF052065
Ostrea conchaphila (Carpenter, 1857)                      KT317155
Ostrea denselamellosa (Lischke, 1869)                     FJ743511
Ostrea edulis (Linnaeus 1758)                             KJ818215

Ostrea futamiensis (Seki, 1929)                           LC051609
Ostrea libella (Weisbord, 1964)
Ostrea lurida (Carpenter, 1864)                           KT317226
Ostrea megodon (Hanley, 1846)                             KX364274
Ostrea permollis (G. B. Sowerby II, 1871)                 AF052075
Ostrea puelchana (d'Orbigny, 1842)                        AF052073
Ostrea equestris (Say, 1834)                              KT317198

Ostrea stentina (Payraudeau, 1826) A

Ostrea stentina (Payraudeau, 1826) B

Ostrea weberi (Olsson, 1951)                              AY376602
Planostrea pestigris (Hanley, 1846)                       KC847125
Pustulostrea australis (Lamarck, 1819)
Pustulostrea pseudangulata (Lamy, 1930)
Saccostreinae
Saccostrea circumsuta (Gould, 1850)
Saccostrea cucullata (Born, 1778) A                       AY247381

Saccostrea cucullata (Born, 1778) B                       AF458906

Saccostrea cucullata (Born, 1778) C                       AY247380
Saccostrea cucullata (Born, 1778) D                       AF458901
Saccostrea cucullata (Born, 1778) E                       AY247387
Saccostrea cucullata (Born, 1778) G                       AY247385
Saccostrea cucullata (Born, 1778) H                       LCI11250
Saccostrea cucullata (Born, 1778) I                       LCI11214
Saccostrea echinata (Quoy & Gaimard, 1835)                KC847127
Saccostrea glomerata (Gould, 1850)                        AF353101
Saccostrea kegaki (Torigoe & Inaba, 1981)                 LCI11266
Saccostrea malabonensls (Faustino, 1932)                  LC005440

Saccostrea mordax (Gould, 1850) A                         AY247323
S.mordax (Gould, 1850) B                                  AY247339
S. mordax (Gould, 1850) C                                 AB898224
Saccostrea mytiloides (Lamarck, 1819)                     AB898228
Saccostrea palmula (Carpenter, 1857)                      FJ768516

Saccostrea scyphophilla (Peron & Lesueur, 1807)
Saccostrea spathulata (Lamarck, 1819)
Saccostrea suhtrigona (G. B. Sowerby II, 1871)
Striostreinae
Striostrea demiculata (Born, 1778)
Striostrea margaritacea (Lamarck, 1819)                   LT220869
Striostrea prismatica (Gray, 1825)                        KT317423

Species                                     Distribution/note

Pycnodonteinae
Empressostrea koslini
(Huber & Lorenz 2007)                       South China Sea
Hyotissa hyotis (Linnaeus 1758)             Indo-Paciflc, eastern
                                            Pacific, Madagascar.
                                            Possibly 3 species
                                            per 16S
Hyotissa fischeri (Dall, 1914)              Mexico to Galapagos
Hyotissa imbrkata (Lamarck, 1819)           China, Japan
Hyotissa inermis (Sowerby II, 1871)         Red Sea, HI.
                                            Relationship with H.
                                            imbrkata not clear
Hyotissa megintyi (Harry 1985)              Tropical eastern and
                                            western Atlantic, TX.
                                            O. thomasi
Hyotissa numisma (Lamarck, 1819)            Indo-Pacific, HI,
                                            East Africa; O.
                                            inaequivalvis
Hyotissa quercina (Sowerby II, 1871)        Mexico to Peru; O.
                                            quercinus
Hyotissa sinensis (Gmelin, 1791)            Andaman and South
                                            China Sea, Polynesia,
                                            Hainan of China
Neopycnodonte cochlear (Poli, 1795)         Circumglobal in lower
                                            latitude, Atlantic,
                                            Indo-Pacific
Neopycnodonte zibrowii
(Gofas, Salas & Taviani,                    2  Azores Archipelago,
                                            NE Atlantic, deep
                                            sea.
                                            May live 500+ years
Pycnodonte taniguchii
(Hayami & Kase 1992)                        Ryukyu Islands,
                                            Japan. Live in
                                            submarine
                                            caves at 20-30 m
Crassostreinae
Crassostrea aequalorialis
(d'Orbigny, 1846)                           Tropical eastern
                                            Pacific. C.
                                            columbiensis?
Crassostrea angulata (Lamarck, 1819)        China, Vietnam.
                                            Introduced to Europe
Crassostrea ariakensis (Fujita, 1913)       China, Korea, Japan.
                                            Crassostrea rivularis
                                            red meat.
                                            endangered
Crassostrea belcheri
(G. B. Sowerby II, 1871)                    China, Vietnam,
                                            Thailand, Pakistan,
                                            Myanmar.
                                            C. gryphoides
Crassostrea bilineata (Roding, 1798)        Indo-Pacific, China, Japan.
                                            C. iredalei?.
Crassostrea brasiliana (Lamarck, 1819)      Brazil, Africa. Crassostrea
                                            gasar, C. paraibanensis
Crassostrea columbiensis (Hanley, 1846)     Eastern Pacific, Gulf of
                                            California to Ecuador
Crassostrea corteziensis (Hertlein, 1951)   Gulf of California to Panama
Crassostrea cultackensis
(Newton & Smith, 1912)                      Indo-Pacific, Philippines
                                            to India. Likely C. belcheri
                                            or
                                            C. dwarkaensis
Crassostrea dactylena
(Iredale, 1939)                             Australia, South China Sea
Crassostrea dianbaiensis
(Xia et al. 2014)                           China, Japan; distinct but
                                            close to C.
                                            iredalei/bilineata
Crassostrea gryphoides
dwarkaensis
(Reece et al. 2008)                         India. Crassostrea
                                            gryphoides, a fossil species
Crassostrea gigas (Thunberg,
1793)                                       China, Korea, Japan.
                                            Introduced worldwide
Crassostrea hongkongensis
(Lam & Morton 2003)                         Southern China. Crassostrea
                                            rivularis white meat
Crassostrea iredalei
(Faustino, 1932)                            Indo-Pacific, China.
                                            Crassostrea bilineata and
                                            possibly >1 species
Crassostrea madrasensis
(Preston, 1916)                             India. Distinct from C.
                                            iredalei. Relationship
                                            to C. bilineata unknown
Crassostrea mangle
(Amaral & Simone, 2014)                     Brazil, no genetic
                                            confirmation
Crassostrea nippona
(Seki, 1934)                                Japan, China
Crassostrea praia
(Ihering, 1907)                             Brazil, endangered
Crassostrea rhizophorae
(Guilding, 1828)                            Caribbean Sea
Crassostrea sikamea
(Amemiya, 1928)                             China, Korea, Japan,
                                            introduced to West Coast of
                                            USA
Crassostrea talonata
(Li & Qi 1994) China                        China. Possibly >1 species
Crassostrea talonata
(Li & Qi 1994) Peru                         Peru
Crassostrea gryphoides
tanintharyiensis (Li et al. 2017)           Tanintharyi, Myanmar. C.
                                            gryphoides, a fossil species
Crassostrea titlipa (Lamarck, 1819)         West Africa. C. gasar, C.
                                            brasiliana, C.
                                            paraibanensisl
Crassostrea virginica (Gmelin, 1791)        Northwestern Atlantic,
                                            Canada. USA, Mexico
Crassostrea zhanjiangensis
(Wu et al. 2013)                            Southern China
Lophinae
Alectryonella plicatula (Gmelin, 1791)      East Africa, Amami, China,
                                            Japan. Possibly >1 species
Lopha cristagalli (Linnaeus 1758)           Red Sea, China, Japan
Dendostrea erenulifera
(G. B. Sowerby II, 1871)                    China, Japan. Dendostrea
                                            sandvichensisl
Dendostrea cristata (Born, 1778)            Australia
Dendostrea folium (Linnaeus 1758)           Indo-Pacific, China, Japan
Dendostrea from (Linnaeus 1758)             Caribbean Sea, USA, Brazil
Dendostrea rosacea (Deshayes, 1836)         Red Sea to Japan. 0.
                                            chenmitzii
Dendostrea sandxichensis
(G. B. Sowerby II, 1871)                   Israel to Hawaii. Dendostrea
                                            erenulifera)
Dendostrea senegalensis (Gmelin, 1791)      West Africa
Dendostrea trapezina (Lamarck, 1819)        Australia
Nicaisolopha tridacnaeformis (Cox, 1927)    Arabia to Melanesia
Ostreinae
Anomiostrea coralliophila (Habe, 1975)      Japan. China, Philippines,
                                            Indo-Pacific
Booneostrea subucula
(Jousseaume in Lamy, 1925)                  Red Sea, Persian Gulf,
                                            Madagascar, Japan.
                                            Ostrea setoensis?
Ostrea fluctigera
(Jousseaume in Lamy, 1925)                  Israel to Japan. Nanostrea
                                            fluctigera
Ostrea algoensis (Sowerby 11, 1871)         South Africa
Ostrea angasi (G. B. Sowerby II, 1871)      Australia. Ostrea edulis
                                            complex
Ostrea angelica (Rochebrune, 1895)          Gulf of California to
                                            Ecuador. Myrakeena angelica
Ostrea atherstonei (Newton, 1913)
Ostrea circumpicta (Pilsbry, 1904)          China, Japan
Ostrea chilensis (Philippi, 1844)           Chile, New Zealand
Ostrea conchaphila (Carpenter, 1857)        Gulf of California to
                                            Panama, south of Punta
                                            Eugenia
Ostrea denselamellosa (Lischke, 1869)       Indonesia, China, Japan,
                                            Korea
Ostrea edulis (Linnaeus 1758)               Europe, Mediterranean Sea,
                                            introduced to USA.
                                            Close to O. angasi
Ostrea futamiensis (Seki, 1929)             Philippines to Japan
Ostrea libella (Weisbord, 1964)             Venezuela
Ostrea lurida (Carpenter, 1864)             North of Punta Eugenia,
                                            Mexico to Alaska
Ostrea megodon (Hanley, 1846)               Gulf of California to Peru.
                                            Undulostrea megodon
Ostrea permollis (G. B. Sowerby II, 1871)   Gulf of Mexico to North
                                            Carolina, USA.
Ostrea puelchana (d'Orbigny, 1842)          Argentina, Brazil.
Ostrea equestris (Say, 1834)                Atlantic and Pacific coast
                                            of Mexico and USA.
                                            Not O. stentina
Ostrea stentina (Payraudeau, 1826) A        Morocco, Portugal, Tunisia,
                                            Japan. Ostrea aupouria,
                                            O. capsa
Ostrea stentina (Payraudeau, 1826) B        Morocco, Portugal, Tunisia,
                                            Japan. Ostrea aupouria,
                                            O. capsa
Ostrea weberi (Olsson, 1951)                Florida and Caribbean Sea.
                                            Teskeyoslrea weberi
Planostrea pestigris (Hanley, 1846)         Indo-Pacific, South China
                                            Sea, Japan
Pustulostrea australis (Lamarck, 1819)
Pustulostrea pseudangulata (Lamy, 1930)     Philippines
Saccostreinae
Saccostrea circumsuta (Gould, 1850)         Sri Lanka to Plynesia
Saccostrea cucullata (Born, 1778) A         Indo-Pacific, Australia,
                                            Japan. Saccostrea
                                            echinata-like

Saccostrea cucullata (Born, 1778) B         Indo-Pacific, Australia,
                                            China, Singapore.
                                            Saccostrea
                                            echinata-like
Saccostrea cucullata (Born, 1778) C         Indo-Pacific, Japan
Saccostrea cucullata (Born, 1778) D         Indo-Pacific, Australia,
                                            China
Saccostrea cucullata (Born, 1778) E         Indo-Pacific, China
Saccostrea cucullata (Born, 1778) G         Indo-Pacific, China
Saccostrea cucullata (Born, 1778) H         Indo-Pacific, Japan.
                                            Saccostrea
                                            ecfunata-like
Saccostrea cucullata (Born, 1778) I         Indo-Pacific, Japan.
                                            Saccostrea
                                            mytiloides'!
Saccostrea echinata
(Quoy & Gaimard, 1835)                      China, Japan
Saccostrea glomerata (Gould, 1850)          Australia
Saccostrea kegaki
(Torigoe & Inaba, 1981)                     China, Japan
Saccostrea malabonensls
(Faustino, 1932)                            China, Japan,
                                            Philippines, Myanmar.
                                            Saccostrea
                                            cucullata F.
                                            2 species
Saccostrea mordax
(Gould, 1850) A                             Indo-Pacific
S.mordax (Gould, 1850) B                    Indo-Pacific
S. mordax (Gould, 1850) C                   Indo-Pacific
Saccostrea mytiloides
(Lamarck, 1819)                             China, Japan.
                                            Saccostrea cucullata
                                            I?
Saccostrea palmula
(Carpenter, 1857)                           Baja California,
                                            Panama and Galapagos
                                            Islands.
                                            O. tubulifera
Saccostrea scyphophilla
(Peron & Lesueur, 1807)                     Red Sea, HI
Saccostrea spathulata
(Lamarck, 1819)                             Indo-Pacific.
                                            Saccostrea cucullata
                                            J?
Saccostrea suhtrigona (G. B.
Sowerby II, 1871)                           Australia
Striostreinae
Striostrea demiculata (Born, 1778)          West Africa, Ghana
Striostrea margaritacea (Lamarck, 1819)     South Africa,
                                            Tropical West Africa
Striostrea prismatica (Gray, 1825)          Mexico to Peru

Species                                        References

Pycnodonteinae
Empressostrea koslini
(Huber & Lorenz 2007)                           Huber and Lorenz (2007)
Hyotissa hyotis (Linnaeus 1758)                 Harry (1985), Bieler et
                                                al. (2004)

Hyotissa fischeri (Dall, 1914)                  Harry (1985)
Hyotissa imbrkata (Lamarck, 1819)               Li and Qi (1994)
Hyotissa inermis (Sowerby II, 1871)             Huber (2010)
Hyotissa megintyi (Harry 1985)                  Harry (1985)
Hyotissa numisma (Lamarck, 1819)                Harry (1985)
Hyotissa quercina (Sowerby II, 1871)            Huber (2010)
Hyotissa sinensis (Gmelin, 1791)                Huber (2010), Li and Qi
                                                (1994)

Neopycnodonte cochlear (Poli, 1795)             Harry (1985)
Neopycnodonte zibrowii
(Gofas, Salas & Taviani, 2009)                  Wisshak et al. (2009)

Pycnodonte taniguchii (Hayami & Kase 1992)      Hayami and Kase (1992)

Crassostreinae
Crassostrea aequalorialis (d'Orbigny, 1846)     Coan and
                                                Valentich-Scott (2012)
Crassostrea angulata (Lamarck, 1819)            Wang et al. (2010)
Crassostrea ariakensis (Fujita, 1913)           Wang et al. (2004a)

Crassostrea belcheri (G. B. Sowerby II, 1871)   Li et al. (2017b)

Crassostrea bilineata (Roding, 1798)            Huber (2010), Xu(1997)
Crassostrea brasiliana (Lamarck, 1819)          Lazoski et al. (2011)
Crassostrea columbiensis (Hanley, 1846)         Harry (1985), Raith et
                                                al. (2016)
Crassostrea corteziensis (Hertlein, 1951)       Harry (1985), Raith et
                                                al. (2016)
Crassostrea cultackensis
(Newton & Smith, 1912)                          Dey (2008), Huber et al.
                                                (2015)

Crassostrea dactylena (Iredale, 1939)           Huber (2010), Huber et
                                                al. (2015)
Crassostrea dianbaiensis (Xia et al. 2014)      Xia el al. (2014)
Crassostrea gryphoides
dwarkaensis (Reece et al. 2008)                 Reece et al. (2008), Li
                                                et al. (2017b)
Crassostrea gigas (Thunberg, 1793)              Harry (1985), Wang et
                                                al. (2010)
Crassostrea hongkongensis
(Lam & Morton 2003)                             Lam and Morton (2003),
                                                Wang et al. (2004a)
Crassostrea iredalei (Faustino, 1932)           Huber (2010), this study

Crassostrea madrasensis (Preston, 1916)         Huber (2010), this study

Crassostrea mangle (Amaral & Simone, 2014)      do Amaral and Simone
                                                (2014)
Crassostrea nippona (Seki, 1934)                Torigoe(1981)
Crassostrea praia (Ihering, 1907)               do Amaral and Simone
                                                (2014)
Crassostrea rhizophorae (Guilding, 1828)        do Amaral and Simone
                                                (2014)
Crassostrea sikamea (Amemiya, 1928)             Wang et al. (2013)
Crassostrea talonata (Li & Qi 1994) China       Li et al. (2017a)
Crassostrea talonata (Li & Qi 1994) Peru        Li et al. (2017a)
Crassostrea gryphoides
tanintharyiensis (Li et al. 2017)               Li et al. (2017b)
Crassostrea titlipa (Lamarck, 1819)             Huber (2010), Huber et
                                                al. (2015)
Crassostrea virginica (Gmelin, 1791)            Harry (1985)
Crassostrea zhanjiangensis
(Wu et al. 2013)                                Wu et al. (2013)
Lophinae
Alectryonella plicatula (Gmelin, 1791)          Torigoe (1981), Li and
                                                Qi (1994)
Lopha cristagalli (Linnaeus 1758)               Torigoe (1981), Li and
                                                Qi (1994)
Dendostrea erenulifera
(G. B. Sowerby II, 1871)                        Torigoe (1981), Li and
                                                Qi (1994)
Dendostrea cristata (Born, 1778)                Huber (2010)
Dendostrea folium (Linnaeus 1758)               Torigoe (1981), Li and
                                                Qi (1994)
Dendostrea from (Linnaeus 1758)                 Huber (2010)
Dendostrea rosacea (Deshayes, 1836)             Huber (2010)
Dendostrea sandxichensis
(G. B. Sowerby II, 1871)                        Huber (2010)
Dendostrea senegalensis (Gmelin, 1791)          Huber (2010)
Dendostrea trapezina (Lamarck, 1819)            Huber (2010)
Nicaisolopha tridacnaeformis (Cox, 1927)        Huber (2010)
Ostreinae
Anomiostrea coralliophila (Habe, 1975)          Huber (2010)
Booneostrea subucula
(Jousseaume in Lamy, 1925)                      Huber (2010)

Ostrea fluctigera
(Jousseaume in Lamy, 1925)                      Huber (2010), Hamaguchi
                                                et al. (2017)
Ostrea algoensis (Sowerby 11, 1871)             Jozefowicz and Foighil
                                                (1998)
Ostrea angasi (G. B. Sowerby II, 1871)          Jozefowicz and Foighil
                                                (1998)
Ostrea angelica (Rochebrune, 1895)              Harry (1985), Raith et
                                                al. (2016)
Ostrea atherstonei (Newton, 1913)               MolluscaBase (2018a,
                                                2018b)
Ostrea circumpicta (Pilsbry, 1904)              Hamaguchi et al. (2014),
                                                Xu (1997)
Ostrea chilensis (Philippi, 1844)               Jozefowicz and Foighil
                                                (1998)
Ostrea conchaphila (Carpenter, 1857)            Raith et al. (2016)
Ostrea denselamellosa (Lischke, 1869)           Torigoe (1981), Li and
                                                Qi (1994)
Ostrea edulis (Linnaeus 1758)                   Huber (2010), this study

Ostrea futamiensis (Seki, 1929)                 Huber (2010)
Ostrea libella (Weisbord, 1964)                 Huber (2010)
Ostrea lurida (Carpenter, 1864)                 Harry (1985), Raith et
                                                al. (2016)
Ostrea megodon (Hanley, 1846)                   Harry (1985), Li et al.
                                                (2017a)
Ostrea permollis
(G. B. Sowerby II, 1871)                        Jozefowicz and Foighil
                                                (1998)
Ostrea puelchana (d'Orbigny, 1842)              Jozefowicz and Foighil
                                                (1998)
Ostrea equestris (Say, 1834)                    Raith et al. (2016),
                                                this study

Ostrea stentina (Payraudeau, 1826) A            Lapegue et al. (2006)

Ostrea stentina (Payraudeau, 1826) B            Lapegue et al. (2006)

Ostrea weberi (Olsson, 1951)                    Harry (1985)
Planostrea pestigris (Hanley, 1846)             Harry (1985), Li and Qi
                                                (1994)
Pustulostrea australis (Lamarck, 1819)          MolluscaBase (2018a,
                                                2018b)
Pustulostrea pseudangulata (Lamy, 1930)         Huber(2010)
Saccostreinae
Saccostrea circumsuta (Gould, 1850)             Huber (2010)
Saccostrea cucullata (Born, 1778) A             Lam and Morton (2006),
                                                Sekino
                                                and Yamashita (2016)
Saccostrea cucullata (Born, 1778) B             Lam and Morton (2006),
                                                Sekino
                                                and Yamashita (2016)
Saccostrea cucullata (Born, 1778) C             Lam and Morton (2006)
Saccostrea cucullata (Born, 1778) D             Lam and Morton (2006)
Saccostrea cucullata (Born, 1778) E             Lam and Morton (2006)
Saccostrea cucullata (Born, 1778) G             Lam and Morton (2006)
Saccostrea cucullata (Born, 1778) H             Sekino and Yamashita
                                                (2016)
Saccostrea cucullata (Born, 1778) I             Sekino and Yamashita
                                                (2016)
Saccostrea echinata
(Quoy & Gaimard, 1835)                          Li and Qi (1994)
Saccostrea glomerata
(Gould, 1850)                                   Lam and Morton (2006)
Saccostrea kegaki
(Torigoe & Inaba, 1981)                         Torigoe (1981), Lam and
                                                Morton (2006)
Saccostrea malabonensls
(Faustino, 1932)                                Sekino and Yamashita
                                                (2016),
                                                Li et al. (2017b)
Saccostrea mordax
(Gould, 1850) A                                 Lam and Morton (2006)
S.mordax (Gould, 1850) B                        Lam and Morton (2006)
S. mordax (Gould, 1850) C                       Hamaguchi et al. (2014)
Saccostrea mytiloides
(Lamarck, 1819)                                 Hamaguchi et al. (2014)
Saccostrea palmula
(Carpenter, 1857)                               Harry (1985), Raith et
                                                al. (2016)

Saccostrea scyphophilla
(Peron & Lesueur, 1807)                         Huber (2010)
Saccostrea spathulata
(Lamarck, 1819)                                 Sekino and Yamashita
                                                (2016)
Saccostrea suhtrigona
(G. B. Sowerby II, 1871)                        Huber (2010)
Striostreinae
Striostrea demiculata
(Born, 1778)                                    Huber (2010)
Striostrea margaritacea
(Lamarck, 1819)                                 Harry (1985)
Striostrea prismatica
(Gray, 1825)                                    Huber (2010), Raith
                                                et al. (2016)
COPYRIGHT 2018 National Shellfisheries Association, Inc.
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Guo, Ximing; Li, Cui; Wang, Haiyan; Xu, Zhe
Publication:Journal of Shellfish Research
Article Type:Report
Date:Oct 1, 2018
Words:14884
Previous Article:OPPORTUNITIES IN FUNCTIONAL GENOMICS: A PRIMER ON LAB AND COMPUTATIONAL ASPECTS.
Next Article:TECHNIQUES FOR ESTIMATING THE AGE AND GROWTH OF MOLLUSCS: GASTROPODA.
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters