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Phylogeny and phylogeography of the geoduck Panopea (Bivalvia: Hiatellidae).

ABSTRACT

Geoducks (Panopea spp.) are recognized as one of the longest-lived and largest burrowing bivalves. Five extant species support commercial fisheries in different countries, yet their phylogenetic relationships are unclear. Phylogenetic analyses using cytochrome oxidase c subunit I, 28S, and 18S partial sequences on five Panopea spp. were performed to understand existing biogeography and to unravel taxonomic uncertainties in the genus. The cytochrome oxidase c subunit I sequences revealed two major clades. The first clade included Panopea zelandica as a sister taxon of Panopea globosa', the second clade included Panopea abbreviata, Panopea generosa, and Panopea japonica. Contrary to expectations, geographically proximate species (P. generosa and P. globosa) belong to different lineages, and geographically distant species (P. generosa and P. japonica) showed lower genetic distance at nuclear loci, suggesting that P. generosa could be related to the common ancestor of P. japonica. Divergence values for mitochondrial DNA, however, indicated that P. japonica might be regarded as a distinct species. Analyses using both nuclear genes suggest that the ancestral species of P. globosa may have been broadly distributed through the Pacific coast to South America.

KEY WORDS: Panopea, geoduck, phylogeny, phylogeography, evolution, molecular markers

INTRODUCTION

Clams of the genus Panopea comprise the largest and longest-lived of all deep-burrowing bivalves; Panopea generosa can live up to 168 y (Bureau et al. 2002). Specimens are found in intertidal and subtidal marine and estuarine waters, typically buried ~1 m below the substratum surface in sandy or mud sediments (Feldman et al. 2004). The genus Panopea is characterized as having a hinge with one small cardinal tooth in each valve (Cox et al. 1969), and a fully fused siphon and mantle. Other taxonomic traits, such as the shape and depth of the pallial sinus are variable among species (Yonge 1971). The genus Panopea was a cosmopolitan genus during the Triassic, and approximately 150 fossil species have been described. Currently only about 10 living species are found in worldwide temperate to subtropical seas and only five species are the subject of commercial fishing activities (Yonge 1971) (Table 1, Fig. 1).

The taxonomy, phylogeny, evolutionary history, and speciation processes of these clams are poorly defined. For example, Panopea generosa was incorrectly synonymized with the extinct Panopea abrupta for almost 25 y (Vadopalas et al. 2010). The clam Panopea japonica from Japan and South Korea has been variously considered as a synonym species of P. generosa--one of the 85 bivalve species distributed on the American and Asian sides of the Pacific Ocean, or as closely related species (Coan et al. 2000). Similarly, because of the geographic proximity (~700 km) Panopea globosa was described as a variety of P. generosa, endemic to the northern Gulf of California (Dali 1898). In addition, the speciation of P. globosa was thought to be associated with the formation of the Gulf of California (Hertlein & Emerson 1956). Fossils of the Latrania Formation, however, indicate that P. globosa lived in the Imperial Sea, California, during the late Miocene (Scott Rugh, Brian F. Smith and Associates, pers. comm., 2011). In addition, geometric morphometric and genetic analyses reveal the presence of P. globosa on the western shore of the Baja Peninsula (Bahia Magdalena) in the Pacific Ocean (Leyva-Valencia 2012, Leyva-Valencia et al. 2012, Suarez-Moo et al. 2012). The fossil Panopea taeniata, found near Bahia Magdalena and described by Dali (1918), was also long considered a subspecies of P. generosa. Recent morphometric analyses, however, revealed that P. taeniata is a fossil morphotype of P. globosa, changing our understanding of the ancient biogeography of P. globosa from the Miocene to the Pleistocene along California and the Baja California Peninsula (Leyva-Valencia et al. 2013).

The biogeographic history of the Panopea genus in the southern circum-Pacific is likewise incomplete. Two extant species of Panopea occur in New Zealand; Panopea zelandica is distinguished from Panopea smithae by morphological differences such as a more shallow pallial sinus and a more squarely truncated posterior end, and inhabiting shallower depths (Beu & Maxwell 1990), and fossils of Panopea worthingtoni have been found in Cretaceous sediments in both New Zealand and Antarctica. Fossils of Antarctic Panopea philippii and Panopea andreae have a close morphological affinity with the extant South American species Panopea abbreviata (Zinsmeister 1984, Studencka 1991). These observations suggest a close relationship among Panopea spp. from New Zealand, Antarctica, and South America.

Phylogenetic studies that include the genus Panopea are scarce (Adamkewicz et al. 1997, Taylor et al. 2007). A recent phylogenetic study of three species of Panopea revealed genetic and morphological variation between Panopea globosa from the Gulf of California and Panopea generosa from the Pacific coast of Baja California (Rocha-Olivares et al. 2010). The authors of these studies concluded that these species do not share a recent ancestor, and proposed trans-Pacific dispersal or vicariance followed by subsequent reproductive isolation between Panopea japonica and P. generosa lineages as possible speciation mechanisms.

Genes with lower mutational rates such as 18S and 28S are useful for characterizing relationships between distant taxa and old divergence processes in bivalves (Adamkewicz et al. 1997, Winnepenninckx et al. 1998, Taylor et al. 2007), although cytochrome oxidase c subunit I (CO1) is used frequently to distinguish differences between close species. The goals of the current study were to determine the phylogenetic relationships among commercially fished Panopea spp. using molecular markers to infer ancient (18S and 28S) and recent (CO1) divergences, to propose a hypothesis encompassing both their historical distribution and extant biogeography, and to begin to unravel the taxonomic uncertainties in the genus Panopea.

MATERIALS AND METHODS

Specimens

A total of 52 specimens from five species in the genus Panopea (Fig. 1) were used to obtain individual sequences of the mitochondrial (mtDNA) gene cytochrome oxidase c subunit 1 (CO1), and the nuclear (nDNA) genes 18S and 28S.

GenBank sequences of Hiatella arctica Linnaeus, 1767 (sister genus to Panopea. accession no. NC008451, AM77451 1, AM779685) and two species in the subclass Heterodonta (Mya arenaria Lamarck, 1809, accession no. AF120668, AF120560. FM999792; and Thyasira sarsi Philippi, 1845, accession no. AM706509, AM774485, AM779659) were selected as out-groups.

DNA Amplification and Sequencing

Genomic DNA samples were obtained from ethanolpreserved siphon tissues using DNeasy Tissue Kits (Qiagen Inc.). From every specimen, a fragment of each gene was amplified with specific primers (CO1, LCO1490-HCO1498 [Folmer et al. 1994]; 28S, 28MF-28MR [Taylor et al. 2007]; and 18S, 18SF18SR [Hedin & Maddison 2001]), using polymerase chain reactions (PCR) in a total volume of 50 pL with 2 U Platinum Taq polymerase (Invitrogen Inc.) 100 ng template DNA, 1 pM of each primer, 200 pM of each dNTP, IX PCR buffer, and 2 mM MgCL. The PCR cycles were carried out in an iCycler PCR System (Bio-Rad Laboratories, CA) under the following conditions: initial denaturation for 5 min at 94[degrees]C, followed by 40 cycles of 45 sec at 94[degrees]C, 1 min annealing temperature (45[degrees]C for CO1; 53[degrees]C for 28S and 18S) and 1 min at 72[degrees]C, with a final 10-min extension at 72[degrees]C.

The length and quality of PCR products were visualized in 1.5% agarose gels stained with ethidium bromide. Purification and sequencing was performed in both directions using the Macrogen sequencing service (Macrogen, Inc. Korea).

Phylogenetic Analyses

The data were quality filtered by excluding individuals with less than three high-quality gene sequences from downstream analyses. The complementary DNA sequence strands were edited manually, assembled, and aligned using the software Sequencher 4.10.1 (Gene Codes, Ann Arbor, Ml) using default parameters, and were saved in Nexus format for phylogenetic analyses. The program DnaSP (Librado & Rosas 2009) was used to identify the haplotypes for each gene.

To test for saturation, transitions, and transversions, uncorrected p distances were computed in DAM BE 5.2.18 to verify that the sequences had not experienced enough substitution saturation to obscure phylogenetic relationships (Xia & Lemey 2009). To compare the mutation rates among lineages, Tajima's relative rate test was performed in MEGA 5.03 (Tamura et al. 2011).

The phylogenetic analysis was carried out by using partitioned and complete sequences of each gene (586 bp for CO1, 565 bp for 28S, and 450 bp for 18S), and by using the concatenated set of 1,651 bp. The haplotypes were analyzed with maximum parsimony, Bayesian inference, and maximum likelihood (ML) to estimate tree topology. Maximum parsimony analyses were executed in PAUP 4.10b* (Swofford 2003); node support was assessed via 1,000 bootstrap replicates.

The nucleotide substitution models used in the analyses were chosen for each partition, individual genes, and for the concatenated data set. To determine the best-fit model for Bayesian inference and ML runs, the Akaike information criterion was used as implemented in Modeltest 3.06 (Posada & Crandall 2001, Posada 2009). The ML analysis was performed by a heuristic search with TBR branch swapping and 100 random additions of taxa, performed in PAUP 4.10b*. Node support was obtained by 1,000 bootstrap replicates (Swofford et al. 2001).

Bayesian inference was explored using the program MrBayes 3.1.1 (Ronquist & Huelsenbeck 2003) using four Markov chains and 5,000,000 generations sampled every 100 generations. The ML analyses were carried out using GARLI O. 951 (Zwickl 2006), RAxML GUI vl.l (Silvestro & Michalk 2011), and Phylogeny.fr (Dereeper et al. 2008) to compare results. Phylogenetic trees were visualized using the program Treeview X (Page 1996).

RESULTS

A total of 120 sequences from five species of Panopea (Table 2) were obtained and 35 haplotypes for all analyzed genes were identified. At COL 17 haplotypes with 217 informative sites were found. At 28S, 14 haplotypes with 97 informative sites were obtained, whereas at 18S, only four haplotypes with 258 informative sites were found. The concatenated data set of the mtDNA and nDNA genes contained 23 haplotypes with 751 informative sites.

The best evolutionary model for the concatenated, CO1, and 28S genes was the generalized time-reversible model plus gamma. The Kirnura (1980) model was superior for 18S. The parameters for the concatenated data were substitution number = 6; base frequencies of A = 0.2114, C = 0.2382, G = 0.2817, and T = 0.2685; and gamma distribution shape parameter = 0.5808.

Within the genus Panopea, no saturation signal was observed for individual or concatenated sequences. The saturation by substitution index (0.146) was significantly less than the critical value (0.783) for the concatenated analyses (Xia & Lemey 2009).

The greatest genetic divergence at CO1 was between Panopea globosa and Panopea abbreviata (18.2%), whereas the lowest divergence was between Panopea zelandica and P. abbreviata (10%). A divergence of less than 5% was determined between P. zelandica and P. abbreviata with 28S, whereas the lowest divergence (0.3%) was observed between the northern hemisphere geoducks Panopea generosa and Panopea japonica. In contrast, 18S revealed smaller differences (1.3%) between P. zelandica and its congeners. The clams P. globosa and P. abbreviata still had the lowest divergence (0.2%) and even shared one haplotype; P. generosa and P. japonica also shared one haplotype (Table 3).

Phylogenetic Analyses

Maximum parsimony, Bayesian inference, and ML analyses revealed two major clades using both concatenated and individual genes. The concatenated tree (Fig. 2A) showed a polytomy among Panopea generosa-Panopea japonica Panopea abbreviata, placing Panopea globosa and Panopea zelanclica in one major clade (C1), and P. generosa, P. japonica, and P. abbreviata in a second clade (C2). Similar topology was present for the CO1 tree (Fig. 2B) although with this gene, P. zelanclica was placed as the basal species of the genus. On the 28S tree (Fig. 2C), P. zelanclica was included with P. globosa and a polytomy is shown among P. generosa, P. japonica, and P. abbreviata, whereas the 18S tree (Fig. 2D) showed a basal polytomy among P. globosa, P. zelanclica, and the others. As expected, we found that the relative rates of evolution of the Panopea genes were 18S rRNA < 28S rRNA < CO1.

DISCUSSION

Contrary to expectations based on geographic proximity, Panopea generosa and Panopea globosa belong to distinct lineages. In addition, the geographically distant species P. generosa and Panopea japonica were included in the same clade, and showed lower divergence at both mitochondrial and nuclear loci, suggesting a close evolutionary relationship.

The results from analyzing concatenated and individual genes provide evidence of two principal lineages and reveal surprising phylogenetic relationships within the Panopea genus. Based on the hypothesis of parapatric speciation between Panopea generosa and Panopea globosa, nuclear genes were used to provide molecular evidence of ancient phylogeny between them, and included other species of the genus for a broader comparison.

Phylogenetic analyses reveal that the clade containing Panopea abbreviata, Panopea generosa, and Panopea japonica is consistent among the concatenated mtDNA and nDNA sequences. The concatenated tree also suggests that P. abbreviata and Panopea zelanclica may share a common ancestor. The individual genes, however, did not yield sufficient information to resolve the phylogenetic relationships among boreal and austral congeners. The relationships between Panopea zelanclica and congeners were dependent on the gene analyzed, whereas P. abbreviata appears to have a close phylogenetic relationship with temperate species from the northern hemisphere at both 28S and CO1. Differences among tree topologies may be the result of distinct mutation rates, although other variables such as the evolutionary history of each gene and the phylogenetic algorithms used can influence results.

The species Panopea was a cosmopolitan group during the Triassic period. For example, species such as Panopea glycimeris were widely distributed in the past (Kensley 1974). Extant aggregations of this species now occur from northern Spain to South Africa (Kensley 1976, Rolan 1983, Thomsen et al. 2009, Scotti et al. 2011). Faunal interchange and the speciation process of Panopea zelanclica and Panopea abbreviata may have been favored by geological and climatic events. Before the breakup of the Gondwana landmass ~55 million y ago, New Zealand began separating from Antarctica. During this time, Australian species such as Panopea worthingtoni, Panopea anclreae, and Panopea philippii occurred in New Zealand, Antarctica, and South America. The progressive movement of the southern continents during the Early Cenozoic resulted in the breakup of the Weddellian Province into smaller, discrete biogeographic units; the distribution of paleoaustral molluscs changed as a result of the separation and isolation of New Zealand from Antarctica (Zinsmeister 1982).

Past faunal interchange between South America and New Zealand is exemplified by Xymene and Antimelatoma. These genera originated in Patagonia and dispersed to New Zealand three different times: during the Oligocene-Early Miocene, Late Miocene-Pliocene, and Pleistocene-Recent, whereas species of the genera Crosseola, Trichosirius, Ataxocerithium, Penion, Xymenella, Zeacuminia, Austromitra, and Eoturris dispersed from New Zealand to Patagonia during the Early Miocene (Del Rio 2004). Before the Tasmanian Seaway and Drake Passage were open and the Isthmus of Panama was closed, ancestors of Panopea zelandica and Panopea abbreviata may have been broadly distributed along the southern Pacific Ocean.

During the Paleogene (23-65 million y ago), global temperatures may have been 10[degrees]C warmer than the current temperature (Lyle et al. 2008), making species flow possible across the Arctic. Modeling studies indicate that ocean circulation during the Cenozoic was similar to the modern geographic distribution of circulation gyres and upwelling systems (Thomas et al. 2006, Lyle et al. 2008, Ogasawara et al. 2008). A close relationship between extant species from the northern hemisphere is consistent with the hypothesis of a correlation between the fauna of northwestern Japan and southern California during the Late Miocene (Otuka 1934), as well as the presence of Panopea generosa fossils in Miocene (Nomura & Niino 1932, Nomura 1935), Pliocene (Yokoyama 1923. Yokoyama 1925), and Pleistocene (Yokoyama 1922) sediments of Japan. Based on the geographic isolation hypothesis, Matsubara (2011) proposed that Panopea japonica has been a distinct species from P. generosa since the Early Miocene, and suggested performing morphology and molecular phylogeny studies to resolve this question. The question of synonymy between P. generosa and P. japonica is a recurrent topic (Coan et al. 2000, Vadopalas et al. 2010).

At CO1, a genetic divergence was observed between Panopea generosa and Panopea japonica of approximately 11%. Divergence values between 10% and 22% at CO1 are considered sufficient to identify separate bivalve species (Therriault et al. 2002, Therriault et al. 2004, Xue et al. 2012), whereas values around of 0.6%-2.0% are typically observed at the intraspecific level (Baldwin et al. 1996, Arnaud et al. 2000, Xue et al. 2012). Thus, the results of the current study are in accord with the hypothesis of Matsubara (2011) that P. generosa and P. japonica are distinct species. However, both nuclear genes revealed low genetic divergence between P. generosa and P. japonica, in accord with the slight 18S gene divergence between P. generosa and P. japonica reported by RochaOlivares et al. (2010). Taken together, the results of the current study suggest ancient gene flow between these boreal species. After carefully ruling out contamination or error through repetition of the analyses, the shared 18S haplotype between P. generosa and P. japonica also supports this hypothesis.

The fossil data reveal that despite the close geographic proximity of Panopea globosa and Panopea generosa, they were distinct species prior to the formation of the Gulf of California. The fossil record also indicates that during the Late Miocene to Pleistocene (~10-0.12 million y ago), P. generosa and P. globosa coexisted in the Salton Trough, California (N. Scott-Rugh, SDNHM, pers. comm., 2010) and in the upper Gulf of California (Judith Terry-Smith, USNMH, pers. comm., 2011). The genetic results from the current study indicate that P. generosa is not the ancestral species of P. globosa, and that they are from distinct basal lineages, given the 17% divergence at COL Results similar to these were obtained using ITS and 18S rDNA sequences (Rocha-Olivares et al. 2010). Because of the current lack of knowledge of Panopea biogeography, the possibility cannot be excluded that extant aggregations of both species occur in sympatry along the Baja Peninsula.

Knowledge of the historical geographic distribution of Panopea globosa is unknown. However, P. globosa fossils collected from Miocene (SDNHM 97243) Pliocene (SDNHM 12085, SDNHM 12104), and Pleistocene (USNMllS.ll, USNM86SJ10, and SDNHM2555-108) sediments in southern California, the Gulf of California, and along the Pacific coast of southern Baja California indicate that P. globosa had a wide geographic distribution before the last glacial period. Valves of P. globosa have also been found in Nayarit, Mexico (SBMNH 135157) and Tumbes, Peru (SBMNH 149357); however, there are no known extant aggregations at these locales. Other bivalves, such as Atrina maura and Argopecten ventricosus, have a distribution range from the Baja Peninsula to Peru (Keen 1971).

Both the genetic affinity between Panopea globosa and Panopea zelandica at 28S, and the shared 18S haplotype between P. globosa and Panopea abbreviata suggest the possibility of a wide-range, warm-water Panopea clade distinct from a cold-water clade. As Smith (1991) proposed for several bivalve species, it is speculated that the ancestral species of P. globosa dispersed from the western Atlantic to the eastern Pacific by seaways across southern Costa Rica and Panama.

Gene flow between eastern Pacific and western Atlantic fauna has been proposed previously (e.g., Rathbun 1918, Marko 2005, Poupin et al. 2005). Before the formation of the Isthmus of Panama, the Atlantic Ocean was a considerably narrower ocean basin than today, and current-mediated larval transport across it may have been feasible during the life span of marine planktonic larvae (Woodring 1982, Schubart et al. 2005). The marine fauna interchange between the Caribbean and the eastern Pacific may have been influenced not only by the closure of the Isthmus of Panama, but also by climate shifts in the Arctic region and the concomitant changes to current systems of the Pacific and Atlantic oceans (Ogasawara et al. 2008).

The only subtropical species known in the genus Panopea- Panopea globosa-had the greatest number of autapomorphies at CO1 (49), whereas Panopea generosa and Panopea japonica had only 22 at the same gene. This difference between tropical and temperate species might be related to environmental adaptations and life cycle differences. Studies of reproductive biology indicate that P. globosa is well adapted to warm temperatures; their reproductive cycle commences in late summer, when sea surface temperatures reach 28[degrees]C, and spawning occurs during winter months, when temperatures are close to 20[degrees]C (Aragon-Noriega et al. 2007). Conversely, P. generosa spawning peaks in late spring and early summer at temperatures closer to 12[degrees]C (Goodwin & Pease 1989, Aragon-Noriega et al. 2007, Arambula-Pujol et al. 2008). The maximum age recorded for P. globosa is 47 y (Gonzalez-Pelaez et al. 2013) whereas P. generosa can live as long as 168 y (Bureau et al. 2002). Nucleotide substitution rates can be correlated with species body size, metabolic rate, generation time, and environmental temperature (Gillooly et al. 2005, Bromham 2009). Thomas et al. (2010) observed that invertebrate species with shorter generation times exhibited greater substitution rates. Adaptation to warmer temperatures and the shorter generation time for P. globosa may likewise be correlated with a greater number of private mutations than its congeners.

Both morphology and genetics have been used to elucidate the taxonomy and phylogeny of bivalves (Giribet & Wheeler 2002, Giribet & Distel 2003, Kappner & Bieler 2006, Owada 2007). Although the general Panopea morphotype is a successful adaptation given that no significant morphological changes are evident during the past 50,000,000 y, species in the genus Panopea can be readily differentiated using shell morphological characteristics (Leyva-Valencia 2012, Leyva-Valencia et al. 2012, Leyva-Valencia et al. 2013). The current results indicate that Panopea congeners can also be discriminated via high interspecific genetic variation.

Based on the results of this study, it is hypothesized that the early evolution of Panopea occurred in two main lineages. One lineage, associated with colder waters, includes Panopea abbreviata, Panopea generosa, and Panopea japonica. The second lineage, associated with warmer waters, includes the subtropical species Panopea globosa and the geographically distant species Panopea zelandica.

It is inferred that the ancestor of Panopea globosa was widely distributed during the Middle Miocene, when the Salton Sea was connected with the Pacific Ocean the proto-Gulf of California opened and the Baja California Peninsula began its separation from mainland Mexico (Helenes & Carreno 1999). This hypothesis will be tested in future studies to help elucidate the evolution of the genus Panopea.

ACKNOWLEDGMENTS

The authors thank Sergio Gonzalez (CIBNOR) and Sergio Perez (CEDO) for providing technical help with sampling. They are grateful to Enrique Morsan, Brooke McVeigh. Kevin Heasman, Emilio Rolan, Paul Valentich Scott, Francisco Fonseca, Tizoc Moctezuma, Concepcion Enciso, Alberto Aragon, Edgar Alcantara, Humberto Garcia, Gianfranco Scotti, Iku Kiryu. Nick King, and Ellie Watts for generously donating tissue samples for this study. They thank paleontologists Tom Dernere and N. Scott-Rugh for providing space in their facilities for their work at the San Diego Natural History Museum. They are indebted to Amanda Lawless, Yolanda Villacampa, Judith Terry Smith, Barbara Studencka, and Claudia del Rio for providing valuable information about and images of Panopea fossils. They thank Miguel Cordoba, Diana Dorantes, and Gopal Murugan (CIBNOR); Gabriela Navas (Moss Landing Marine Laboratory); Claire Olson, Emma Timmins-Schiffman, Kristina Straus, and Fred Utter (University of Washington); and two anonymous referees for providing detailed editorial comments and constructive criticisms that greatly improved the manuscript. The research was funded by Consejo Nacional de Ciencia y Tecnologia (CONACYT, grant 106905). ILV was the recipient of a CONACYT doctoral fellowship (no. 98412).

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IGNACIO LEYVA-VALENCIA, (1) PEDRO CRUZ-HERNANDEZ, (1) SERGIO T. ALVAREZ-CASTANEDA, (1) * DELIA I. ROJAS-POSADAS, (1) MIGUEL M. CORREA-RAMIREZ, (2) BRENT VADOPALAS (3) AND DANIEL B. LLUCH-COTA (1)

(1) Centro de Investigaciones Biologicas del Noroeste, Instituto Politecnico Nacioncd No. 195, Col. Playa Palo de Santa Rita Sur, Apdo. Postal 128, La Paz, B.C.S. 23096, Mexico; (2) Centro Interdisciplinarity de Investigacionpara el Desarrollo Integral Regional, Unidad Durango, Instituto Politecnico National, Calle Sigma 119 Fracc. 20 de Noviembre II Durango, Durango 34220, Mexico; (3) School of Aquatic and Fishery Sciences, University of Washington, 1122 NE Boat Street, Seattle, WA 98105

* Corresponding author. E-mail: sticul@cibnor.mx

DOI: 10.2983/035.034.0104

TABLE 1.

Living species of Panopea recognized around the world.

Species              Authority                Distribution range

Panopea glycimeris   von Born, 1778           Northwestern Spain;
                                                Mediterranean Sea to
                                                South Africa
Panopea australis    Sowerby, 1833            Southern and eastern
                                                Australia
Panopea zelandica    Quoy and Gaimard, 1835   New Zealand
Panopea smithae      Powell, 1950             New Zealand
Panopea abbreviata   Valenciennes, 1839       Southwestern Argentina
Panopea japonica     Adams, 1850              Japan Sea
Panopea bitruncata   Conrad, 1872             North Carolina to the
                                                Gulf of Mexico
Panopea generosa     Gould. 1850              Southern Alaska to
                                                Mexico
Panopea globosa      Dali, 1898               Gulf of California,
                                                Mexico

Species              Citation

Panopea glycimeris   Lensky (1974). Rolan (1983),
                       Scotti et al. 2011

Panopea australis    Grove (2011)

Panopea zelandica    Breen et al. (1991)
Panopea smithae      Breen et al. (1991)
Panopea abbreviata   Morsan & Ciocco (2004)
Panopea japonica     Coan et al. (2000)
Panopea bitruncata   Robertson (1963), John Slapcinsky
                       (FLMNH pers. comm.)
Panopea generosa     Goodwin & Pease (1989), Coan et al.
                       (2000), Cadien & Lovell (2008)
Panopea globosa      Aragon-Noriega et al. (2007),
                       Rocha-Olivares et al. (2010)

TABLE 2.
Haplotypes identified within the five species of the genus Panopea
from Bahia Magdalena, Puerto Penasco, Guaymas, San Felipe, Gulf of
San Mafias, New Zealand, Ensenada, California, Alaska, Washington,
and Japan for mitochondrial (COl) and nuclear genes (28S and 18S).

Species               Locality   Sample    Voucher ID   Haplotype
                                                           CO1

Panopea globosa          BM        BM1         1           HCO1
P. globosa               BM        BM2         2           HCO9
P. globosa               BM       BIVI3        3           HCO1
P. globosa               BM        BM4         4           HCO1
P. globosa               BM        BM5         5           HCO1
P. globosa               PP        PP1         8           HCO1
P. globosa               PP        PP2         9           HCO3
P. globosa               PP        PP3         10          HCOS
P. globosa               PP        PP4         11          HCO1
P. globosa               PP        PP5         12          HCO7
P. globosa               GU        GUI         13          HCO6
P. globosa               GU        GU2         14          HCO1
P. globosa               GU        GU3         15          HCO1
P. globosa               GU        GU4         16          HCO1
P. globosa               GU        GU5         17          HCO8
P. globosa               SF        SF3         6           HCO4
P. globosa               SF        SF5         7           HCO2
Panopea abbreviata      GSM       Pabbl        36         HCO16
P. abbreviata           GSM       Pabb2        37         HCO17
P. abbreviata           GSM       Pabb3        38         HCO17
P. abbreviata           GSM       Pabb4        39         HCO16
P. abbreviata           GSM       Pabb5        40         HCO16
Panopea zelandica        NZ       NZel3        18         HCO10
P. zelandica             NZ       NZel4        19         HCO10
P. zelandica             NZ       NZel5        20         HCO10
Panopea generosa        ENS       Ensl         21         HCO11
P. generosa             ENS       Ens2         22         HCO11
P. generosa             ENS       Ens3         23         HCO11
P. generosa             ENS       Ens4         24         HCO11
P. generosa             CAL       Call         25         HCO12
P. generosa             CAL       Cal2         26         HCO11
P. generosa             ALA       Ala77        27         HCO11
P. generosa             ALA       Ala80        28         HCO11
P. generosa             ALA       Ala82        29         HCO13
P. generosa             ALA       Ala83        30         HCO11
P. generosa             WASH     Wash97        31         HCO12
P. generosa             WASH     Wash101       32         HCO11
Panopea japonica        JAP       Japl         33         HCO14
P. japonica             JAP       Jap2         34         HCO14
P. japonica             JAP       Jap3         35         HCO15
Hiatetla arctica         --        --          --         HCO18
Mya arenaria             --        --          --         HCO19
Thyasira sarsi           --        --          --         HCO20

Species                 GenBank       Haplotype      GenBank
                      accession no.    28S rRNA    accession no.

Panopea globosa         JQ071876         H286        JQ071883
P. globosa              JQ071868         H287        JQ071886
P. globosa              JQ071876         H289        JQ071882
P. globosa              JQ071876         H288        JQ071884
P. globosa              JQ071876         H286        JQ071883
P. globosa              JQ071876         H282        JQ071891
P. globosa              JQ071878         H285        JQ071885
P. globosa              JQ071872         H284        JQ071889
P. globosa              JQ071876         H282        JQ071891
P. globosa              JQ071862         H282        JQ071891
P. globosa              JQ071876         H281        JQ071892
P. globosa              JQ071876         H281        JQ071892
P. globosa              JQ071876         H281        JQ071892
P. globosa              JQ071876         H281        JQ071892
P. globosa              JQ071865         H281        JQ071892
P. globosa              JQ07187I         H283        JQ071890
P. globosa              JQ071877         H284        JQ071889
Panopea abbreviata      JQ071864        H2813        JQ071887
P. abbreviata           JQ071866        H2813        JQ071887
P. abbreviata           JQ071866        H2813        JQ071887
P. abbreviata           JQ071864        H2813        JQ071887
P. abbreviata           JQ071864        H2813        JQ071887
Panopea zelandica       JQ071875        H2814        JQ071888
P. zelandica            JQ071875        H28I4        JQ071888
P. zelandica            JQ071875        H2814        JQ071888
Panopea generosa        JQ071867        H2810        JQ071879
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071869        H2810        JQ071879
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071867        H2811        JQ071880
P. generosa             JQ071863        H2811        JQ071880
P. generosa             JQ071867        H2810        JQ071879
P. generosa             JQ071869        H2810        JQ071883
P. generosa             JQ071867        H2811        JQ071880
Panopea japonica        JQ071873        H2812        JQ07I88I
P. japonica             JQ071873        H2812        JQ071881
P. japonica             JQ071874        H2812        JQ071881
Hiatetla arctica        NC008451        H2815        AM779685
Mya arenaria            AF120668        H2816        FM999792
Thyasira sarsi          AM706509        H2817        AM779659

Species                 Haplotype         GenBank       Concatenated
                         18S rRNA       accession no.     haplotype

Panopea globosa            H181           JQ071895          HCN10
P. globosa                 H181           JQ071895          HCN1I
P. globosa                 H181           JQ071895          HCN13
P. globosa                 H181           JQ071895          HCN12
P. globosa                 H181           JQ071895          HCN10
P. globosa                 H181           JQ071895          HCN5
P. globosa                 H181           JQ071895          HCN9
P. globosa                 H181           JQ071895          HCN8
P. globosa                 H181           JQ071895          HCN5
P. globosa                 H181           JQ071895          HCN3
P. globosa                 H181           JQ071895          HCN2
P. globosa                 H181           JQ071895          HCN1
P. globosa                 H181           JQ071895          HCN1
P. globosa                 H181           JQ071895          HCN1
P. globosa                 H181           JQ071895          HCN4
P. globosa                 H182           JQ071897          HCN6
P. globosa                H182 *          JQ071897          HCN7
Panopea abbreviata        H182 *          JQ071898          HCN23
P. abbreviata              H182           JQ071898          HCN22
P. abbreviata              H182           JQ071898          HCN22
P. abbreviata              H182           JQ071898          HCN23
P. abbreviata              H182           JQ071898          HCN23
Panopea zelandica          H183           JQ071896          HCN14
P. zelandica               H183           JQ071896          HCN14
P. zelandica               H183           JQ071896          HCN14
Panopea generosa           H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN21
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN15
P. generosa                H184           JQ071893          HCN17
P. generosa                H184           JQ071893          HCN17
P. generosa                H184           JQ071893          HCN16
P. generosa           H184 ([dagger])     JQ071893          HCN18
Panopea japonica      H184 ([dagger])     JQ071894          HCN19
P. japonica                H184           JQ071894          HCN19
P. japonica                H184           JQ071894          HCN20
Hiatetla arctica           H185           AM774511           --
Mya arenaria               H186           AF120560           --
Thyasira sarsi             H187           AM774485           --

ALA, Alaska; BM, Bahia Magdalena: CAL, California; ENS, Ensenada;
GSM, Gulf of San Matias; GU, Guaymas; JAP, Japan; NZ, New Zealand;
PP, Puerto Penasco; SF, San Felipe; WASH, Washington, Samples in bold
type were used to characterize the haplotypes (bold). * One shared
haplotype between Panopea globosa and Panopea abbreviate, ([dagger])
One shared haplotype between Panopea generosa and Panopea japonica.

TABLE 3.

Divergence percentages within and between Panopea spp. at
mitochondrial and nuclear genes using the Kimura two-parameter model.

                           Cytochrome oxidase c subunit I

                Panopea    Panopea    Panopea      Panopea    Panopea
Species         generosa   globosa   abbreviata   zelandica   japonica

P. generosa       0.16
P. globosa        17.7       0.4
P. abbreviata     12.6      18.2         0.1
P. zelandica      12.6      15.1        10.0         --
P. japonica       10.9      17.0        11.6        10.0        0.3

28S rRNA

  P. generosa      0.3
  P. globosa       3.1       0.4
  P. abbreviata    2.1       3.8
  P. zelandica     3.8       4.0         4.6         --
  P. japonica      0.3       3.1         2.1         3.7         --

18S rRNA

  P. generosa      --
  P. globosa       2.6       --
  P. abbreviata    2.6       0.2         --
  P. zelandica     1.3       1.3         1.3         --
  P. japonica      --        2.6         2.6         1.3         --

--No observed genetic divergence.
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