Morphological and genetic variation indicate cryptic species within Lamarck's little sea star, Parvulastra (=Patiriella) exigua.
Asterinid sea stars are a mainly Indo-Pacific family (Rowe and Gates, 1995) that includes multiple clades with evolutionarily convergent modifications of the mating system, fertilization ecology, egg and clutch size, larval form, planktonic dispersal ability, and other aspects of the typical sea star complex life cycle (Byrne, 1992; Byrne and Cerra, 1996; Hart et al., 2003; Waters et al., 2004b). Documenting the reproductive variation among asterinids has led to a series of recent efforts to understand the developmental bases for these differences (e.g., Byrne et al., 1999; Villinski et al., 2002; Byrne, 2005) and their ecological or population genetic consequences (Hunt, 1993; Waters and Roy, 2004; Colgan et al., 2005) and to a reconsideration of asterinid classification based on both morphological and molecular characters (O'Loughlin, 2002; O'Loughlin et al., 2002, 2003; O'Loughlin and Waters, 2004). The comparative basis for this work has been molecular phylogenies for asterinid species groups (Hart et al., 1997, 2004; O'Loughlin et al., 2003; Waters et al., 2004b). A predictable consequence (Knowlton, 1993) of the combination of molecular and reproductive surveys has been the discovery of considerable cryptic species diversity (Hart et al., 1997, 2003; O'Loughlin, 2002; O'Loughlin et al., 2002, 2003; Dartnall et al., 2003; Waters et al., 2004a). Some cryptic species groups have divergent molecular characters and subtle but identifiable adult morphological differences but similar reproductive traits (O'Loughlin et al., 2002, 2003), while other cryptic species groups have surprisingly divergent reproduction without significant and obvious divergence in adult morphology (Byrne et al., 2003; Hart et al., 2003).
The documentation and measurement of cryptic species diversity in the oceans has important ecological, evolutionary, and conservation implications (Knowlton, 1993, 2000; Mikkelsen and Cracraft, 2001). Here we summarize evidence for cryptic species diversity within the widespread and abundant south-temperate asterinid Parvulastra exigua. We surveyed a key taxonomic and reproductive character (the location of the gonopores) in museum collections from Africa, Australia, and several oceanic islands. This survey includes the rediscovered type specimen series, which we use as the basis for reconsidering the taxonomy of this cryptic species group. Our survey indicated that some African and island populations include a species with oral gonopores (and benthic egg masses) that is probably conspecific with Australian P. exigua, plus at least one other species (not found in Australia) with aboral gonopores (and possibly planktonic spawning of gametes). In light of this discovery and the propensity for the presence of cryptic morphospecies in the Asterinidae (references above), we reconsidered mitochondrial DNA (mtDNA) sequence data from a recent study (Waters and Roy, 2004) of genetic variation among African, Australian, and island populations of P. exigua with divergent mtDNA haplotypes. We suggest that these data are also consistent with the co-occurrence of multiple species in some parts of the P. exigua range.
Classification and Biology of Lamarck's Little Sea Star
What is Parvulastra exigua?
Lamarck (1816) described Asterias exigua as a little pentagonal star from the "mers d'Ameriques," though it is clear that all of his specimens were from the eastern (Africa) rather than the western (South America) Atlantic Ocean. Extensive revision and synonymization has followed (see Dartnall, 1971; Walenkamp, 1990). Perrier (1875) noted considerable taxonomic confusion surrounding this species; he concluded that Asterina exigua Lamarck, A. kraussii Gray, and Asteriscus pentagonus Muller and Troschel are conspecific. Whitelegge (1889) noted that the species has abbreviated larval development. Verrill (1913) assigned Asterina exigua and several other species to the new genus Patiriella (but this change was often ignored, and later work frequently refers to Asterina exigua). Mortensen (1921) emphasized the presence of orally directed gonopores (Fig. 1A) in the adult P. exigua and suggested that the taxon includes several species. H. L. Clark (1923) then described a new species, Asterina dyscrita, similar to and co-occurring with P. exigua (e.g., at False Bay, South Africa), but having aboral gonopores: this was the first confirmation that the entity exigua in southern Africa might include more than one species. Unfortunately, and in spite of his earlier observations of different gonopore phenotypes, Mortensen (1933) subsequently placed A. dyscrita in synonymy with P. exigua. Many other South African workers did differentiate dyscrita from exigua (on the basis of size, habitat, surface texture, and color; C. Griffiths, University of Cape Town; pers. comm.), but lumped within the latter taxon individuals with striking phenotype differences (Stephenson et al., 1937, 1938, 1939; Bright, 1938, Eyre and Stephenson, 1938, 1944; Eyre et al., 1938; Eyre, 1939; Day and Morgans, 1956; MacNae, 1957; Kalk, 1958; Balinsky, 1969; Day, 1969; Penrith and Kensley, 1970; Stephenson and Stephenson, 1972). Dartnall (1971) noted P. exigua specimens with and without oral gonopores from South Africa, reported that the type material of the species had apparently been lost, and raised a neotype for the species. A. M. Clark (1974) then confirmed the aboral location of gonopores in H. L. Clark's dyscrita.
The most recent considerations of P. exigua suggest that additional cryptic variation might be present within this taxon. Walenkamp (1990) proposed that southern African collections of P. exigua might also include forms with aboral gonopores, including dyscrita and pentagona Muller and Troschel. Dartnall et al. (2003) removed the pantropical exiguoids (including pentagona) from Patiriella to the new genus Cryptasterina, and O'Loughlin (in O'Loughlin and Waters, 2004) removed several temperate exiguoids from Patiriella to a new genus as Parvulastra exigua, P. vivipara, P. parvivipara, P. dyscrita, and P. calcarata. The revision of asterinid genera by O'Loughlin and Waters (2004) was inspired by a series of molecular phylogenetic studies (especially Waters et al., 2004b) that did not include P. dyscrita. However, O'Loughlin and Waters (2004) noted several morphological characteristics (in addition to the striking difference in gonopore location) that appear to distinguish P. exigua from P. dyscrita.
As a result of this series of changes, the small pentagonal sea stars of southern Africa appear to comprise at least three entities, including Parvulastra dyscrita, P. exigua sensu stricto (s. s.) with oral gonopores (widely distributed in the temperate southern hemisphere), and at least one other species called exigua that has aboral gonopores.
Reproduction and population biology
Reproduction in Parvulastra exigua has been studied in detail only in Australian populations. Adults are simultaneous hermaphrodites, and some evidence for self-fertilization has been found in laboratory studies (Byrne, 1992, 1995). Females lay eggs on the substratum through oral gonopores, two per interradius (Fig. 1A), in contrast to free-spawning and internally brooding asterinids, which have aboral gonopores (Fig. 1B; Byrne and Cerra, 1996). The oral location of the gonopores facilitates deposition of sticky egg masses onto rocky surfaces, as in species of Aquilonastra and Asterina that have convergently evolved this mode of development (Byrne and Cerra, 1996). Differences in this character are diagnostic for asterinid species (Byrne and Cerra, 1996). Individual sea stars--including individuals with radii as small as 4 mm--always have all aboral or all oral gonopores (Byrne, 1992); conspecific individuals always have the same character state; and individuals that differ in this character are always members of different biological species with different modes of reproduction.
Morphogenesis within the egg mass is followed by hatching and attachment to the substrate via a specialized adhesive organ that is found in most other sea star families and is especially well-developed in P. exigua larvae (Byrne, 1995). In spite of the absence of a planktonic larval stage in the life cycle, P. exigua has a surprisingly broad geographic distribution (Dartnall, 1971; Waters and Roy, 2004; Colgan et al., 2005). Populations occur as far south as Kerguelen Island (Dartnall, 1971; unpubl. obs.). Their west-to-east distribution includes St. Helena in the south Atlantic, southern Africa, Amsterdam and St. Paul Islands in the southern Indian Ocean, southeastern Australia and Tasmania, and Lord Howe Island in the Pacific. Adults of this species may be capable of long-distance dispersal by rafting (e.g., Jo-hannesson, 1988) on structures such as macroalgae dispersed by the West Wind Drift (or Antarctic Circumpolar Current), the major west-to-east pattern of circulation of the Southern Ocean (Mortensen, 1933; Fell, 1962; Munoz et al., 2004; Waters and Roy, 2004). Recent phylogeographic studies show strong local haplotype differentiation and imply limited gene flow between populations (Waters and Roy, 2004; Colgan et al., 2005).
Materials and Methods
We examined collections of Parvulastra exigua held at the Musee Nationale d'Histoire Naturelle (MNHN, Paris), Nationaal Natuurhistorisch Museum (NNM, Leiden), Zoological Museum (ZMUC, Copenhagen), British Museum (BMNH, London), National Museum of Natural History (NMNH, Washington, DC), and Museum Victoria (MV, Melbourne) (Table 1). These collections included specimens from St. Helena, southern Africa, Amsterdam Island, St. Paul Island, Kerguelen Island, and southern Australia. The presence of oral or aboral gonopores was scored (Fig. 1). Some specimens could not be scored because of poor preservation and are thus listed as uncertain; we include these individuals in totals to indicate the comprehensive nature of the survey.
We obtained the original sequence alignment of Waters and Roy (2004) from TreeBase (SN1606-4917). It includes sequences from the cytochrome c oxidase subunit I (COI) gene, plus a second fragment composed of part of the 12S rDNA gene, a tRNA gene, and the putative control region. The alignment consists of 24 haplotypes of 1603 nucleotide sites from 43 individuals. The haplotypes come from three sites (with two-letter abbreviations) in southern Africa (Cape Town on the Atlantic Ocean, CT; Port St. Johns and Durban on the Indian Ocean, PJ, DB), eight sites in Australia from Victoria (Flinders, VF; Williamstown, VW; Cape Otway, VO), New South Wales (Mona Vale, NM; Bondi, NB), and Tasmania (Woodbridge, TW; Eaglehawk Neck, TE; Taranna, TT), and the oceanic islands St. Helena (Atlantic, SH), Amsterdam Island (Indian, AM), and Lord Howe Island (Pacific, LH).
We used PAUP* ver. 4.0b10 (Swofford, 2002) to calculate Kimura two-parameter genetic distances among haplotypes (as in Waters and Roy, 2004). We used TCS version 1.21 (Clement et al., 2000) to construct parsimony haplotype networks. For most analyses we used the 95% plausible connection limit. We dropped one haplotype from Bondi (NB.4) for which more than half the characters (including all COI sites) were missing. We treated gaps as missing data. We used the haplotype network analysis to test our inference of multiple morphological species by asking whether the haplotype data form multiple separate networks corresponding to cryptic species.
The application of parsimony network methods rather than tree-based methods may be a significant improvement in the use of haplotype data to identify morphologically cryptic species (e.g., Templeton, 2001). Indeed, network methods for intraspecific phylogeography have become a key tool for population genetic analysis (Avise, 2004) because they include relevant biological features of sequence evolution (extant ancestral sequences in sampled populations; real polytomies) that are not elements of tree-based methods developed for species-level phylogenies, and because network methods are largely independent of some other tree-based criteria (strict monophyly, strong nodal support, large genetic distances between clades) that are problematic for tree-based species definitions (Mallet, 1995; Sites and Marshall, 2004).
Network methods assign sampled sequences to the tips or to the interior nodes of an unrooted branching diagram; sequences assigned to interior nodes are assumed to be older than and ancestral to sequences assigned to tips (Posada and Crandall, 2001). The sampled sequences can be connected to each other by some number of unobserved intermediate haplotypes up to a specified level of confidence (the connection limit). The extent of lineage sorting--the extinction of ancestral haplotypes by genetic drift--could be used as an objective benchmark to identify otherwise cryptic species: a single network from a haplotype alignment of a single species in which lineage sorting has been modest; two or more networks from an alignment that consists of sequences from multiple species that have been separated long enough for substantial lineage sorting to render them distinct at the 95% connection limit. This application of parsimony networks might represent a simple but effective implementation of more sophisticated genetic clustering methods that have been advocated as a complement to species definitions based on interbreeding or tree topology (Mallet, 1995; Templeton, 2001; Wiens and Penkrot, 2002).
Examination of Lamarck's rediscovered type specimens in the Musee Nationale d'Histoire Naturelle (MNHN) provided improved understanding of the taxonomy and biogeography of Parvulastra exigua. The syntypes (MNHN EcAs 2356) comprise seven dry specimens accompanied by a series of labels, including some of Lamarck's era and some of Perrier's era, that refer to 18th century descriptions (Linck, 1773; Bruguieres, 1792). The syntypes had been glued to a paper card and are in poor condition. Judicious cleaning of the old glue (by AJD) exposed actinal gonopores directed toward the oral surface--the specific character of note in this account. The specimens are identical to material of P. exigua examined by us (including the now defunct neotype) and by Walenkamp (1990) throughout the known range of the species. Our understanding of the benthic egg-laying life history of this taxon corresponds to Lamarck's exigua. The forms with aboral gonopores include P. dyscrita and at least one undescribed species whose biology is unexplored.
We found some specimens with oral gonopores and others with aboral gonopores in collections of P. exigua from St. Helena (south Atlantic Ocean), Africa, and the southern Indian Ocean islands (Table 1). Aboral gonopores emerged along the dorsal insertion of the interradial pillar. Specimens with oral gonopores are most likely to be conspecific with P. exigua from Australia, which always have oral gonopores and lay benthic egg masses. Some single collections from St. Helena (MNHN 1493) and St. Paul (MNHN 3925) islands contained a mix of individuals with oral and others with aboral gonopores. The majority of specimens had oral gonopores at St. Helena (where we scored many individuals) and in southern Africa (where we scored fewer individuals). Specimens with aboral gonopores were more frequent on Indian Ocean islands. Overall, about 33% of specimens in which the character could be scored had aboral gonopores (but otherwise resembled the P. exigua syntypes), and were unlikely to be conspecific with Australian P. exigua.
Parsimony haplotype network
The 95% connection limit for P. exigua haplotypes was 17 nucleotide substitutions: haplotypes more than 17 steps removed from any other haplotype could not be reliably connected to the rest of the network. As a result, the two AM haplotypes from the mid-Indian Ocean, the three CT haplotypes from southern Africa, and the single SH haplotype from St. Helena in the southern Atlantic Ocean formed three networks separate from each other and from a fourth network that included geographically widespread haplotypes. The results suggest that this sequence alignment includes up to four cryptic species called P. exigua.
The seven Amsterdam Island (AM) and Cape Town (CT) individuals were especially divergent from others (Waters and Roy, 2004). Only at 50 steps (almost 3 times the 95% plausible limit) could these haplotypes be joined to all other haplotypes in a single network. Kimura two-parameter genetic distances between these five haplotypes and other P. exigua (5.2%-7.0%) were comparable to COI and control region genetic distances among congeneric species in other sea star and brittlestar phylogenetic analyses (e.g., Foltz, 1997; Hart et al., 1997; O'Loughlin et al., 2003; Hart and Podolsky, 2005). The genetic distances between AM and CT haplotypes (3.0%-4.5%) were also much larger than the typical range of asterinid conspecific COI genetic distances (< 1%) found in sparse geographic sampling of Cryptasterina species by Hart et al. (2003) and intensive geographic sampling of Meridiastra species by O'Loughlin et al. (2003) and Waters et al. (2004a) and of Australian P. exigua by Colgan et al. (2005). Waters and Roy (2004) found that the AM and CT haplotypes formed the sister group to other sampled populations in a maximum likelihood phylogeny, but with long internal branches leading to distinctive AM and CT clades. Our parsimony network analysis and the large genetic distances suggest that sequence divergence and lineage sorting between these clades has been extensive. This result is consistent with other published studies (see Discussion) in which divergence and lineage sorting between multiple species produces multiple haplotype networks at the 95% connection limit. We conclude tentatively that these five AM and CT haplotypes are not conspecific with other P. exigua (and possibly not conspecific with each other). This conclusion is consistent with the observation of multiple morphological phenotypes (and probably multiple modes of reproduction) in P. exigua samples from African and island populations (Table 1).
The divergence of the St. Helena (SH) haplotype (in four individuals) from some other P. exigua was less striking. This haplotype lay outside the 95% plausible parsimony networks for other haplotypes, and was separated from the AM and CT haplotype networks by large genetic distances (5.8%-6.7%). However, the genetic distances between this SH haplotype and members of the large, widespread network that includes all Australian populations were relatively smaller (1.7%-2.1%), and this haplotype could be connected to the large, widespread haplotype network by relaxing the connection limit from 95% to 90% (25 steps). The SH haplotype formed part of a four-way polytomy with African and Australian haplotypes in the maximum likelihood phylogeny of Waters and Roy (2004).
The fourth haplotype network (31 individuals, 17 haplotypes) included all Australian and Tasmanian samples (Fig. 2). The highest outgroup weight (0.21) was assigned to a haplotype from Tasmania (TW.3), but the small number of connections (2) between TW.3 and other haplotypes suggest that it is not the ancestral haplotype; the program TCS identified TW.3 as the root for the network because it makes two connections to other haplotypes, including one very common haplotype (TW.1) that was found in both Tasmania and in southern Australia (one of only two examples of haplotype sharing between populations in this sequence alignment; Waters and Roy, 2004). Other African (PJ, DB) and island (LH) haplotypes were connected to the network by long terminal branches of 13-17 steps. The large number of substitutions separating these haplotypes from the Australian part of the network, and the lack of haplotypes shared between Africa and Australia, suggests ancient dispersal of this species out of Australia to other African and island populations but without recent substantial gene flow between populations (Waters and Roy, 2004; Colgan et al., 2005). These results are consistent with a widely distributed species (P. exigua s. s.) that includes Australian populations (in which only oral gonopores are found) and some African and island populations (in which oral gonopores occur).
Linking morphology to genotype
We attempted to link the highly divergent haplotype clades to the divergent gonopore phenotypes by examining voucher specimens used for mtDNA sequences (Waters and Roy, 2004). Two of us (MB, AJD) independently examined four accessions from St. Helena (MV F98060; n = 4), Durban (MV F98061; n = 4), Cape Town (MV F98062; n = 4), and Amsterdam Island (MV F98063; n = 2). From the mtDNA haplotypes and network analysis we predicted that (1) the St. Helena and Durban specimens would have oral gonopores similar to closely related Australian populations and to P. exigua s. s.; and (2) the Amsterdam Island and Cape Town specimens would show aboral gonopores or other morphological evidence that they are not conspecific with P. exigua s. s.
Examination of the St. Helena and Durban accessions revealed that oral gonopores were evident in most specimens (and none had visible aboral gonopores); this specific character and the overall appearance of these specimens was consistent with P. exigua s. s. The Durban specimens were difficult to score but could not be conclusively excluded as P. exigua s. s. These results are consistent with the genetic data that link these specimens with Australian populations in which only P. exigua s. s. with oral gonopores have been found.
The four Cape Town individuals were of highly variable quality. In one specimen, lack of soft tissue prevented us from identifying any of the holes on the oral disk as gonopores; in the others, we could tentatively identify 2-4 tissue-bound pores. In the absence of stronger evidence, we conclude that these are not obviously different from P. exigua s. s. In contrast, both of the Amsterdam Island individuals lacked oral or aboral gonopores. In this respect, and in overall appearance, these specimens were not consistent with the P. exigua type series. They did not resemble the other museum accession we examined from Amsterdam Island (BMNH 1975.12.4), nor did they conform to our general notion of the P. exigua morphospecies in Australia. Thus, these data provide mixed evidence for linking one (Amsterdam Island) but not another (Cape Town) highly divergent haplotype clade to the gonopore phenotype that is not found in the P. exigua type series or in Australian populations.
An alternative approach involves new mtDNA sequence data from field (rather than museum) samples in which gonopore phenotypes can be scored unambiguously on the live animal. Extensive sampling and sequencing of individuals from Parvulastra populations around southern Africa includes P. dyscrita plus P. exigua populations where both gonopore phenotypes occur (K. Dunbar, C. Griffiths, M. Bruford, unpubl. data). Future morphological analysis of these specimens will fully reveal the extent of cryptic species diversity and associated life history diversity among these lineages.
Our examination of museum specimens shows that the geographic range of Parvulastra exigua includes two broadly distributed and distinctive gonopore phenotypes. Because all other asterinid species that differ in the location of the gonopores have striking differences in modes of reproduction and larval development (including benthic egg masses in species with oral gonopores), we tentatively conclude that at least two different biological species with different modes of reproduction are present at these African and island sampling locations: P. exigua s. s., which has oral gonopores (and probably larval development in benthic egg masses) and is conspecific with P. exigua in Australia; and one or more additional species not found in Australia, at least one of which has aboral gonopores (and some other mode of reproduction).
Our reconsideration of published mtDNA sequences also suggests the presence of one or more cryptic species. Marine phylogeographers have typically interpreted haplotype samples that break down into separate 95% plausible networks in the way we have: as evidence of multiple species (Lee and OFoighil, 2004; Tarjuelo et al., 2004; Uthicke et al., 2004; Addison and Hart, 2005; Baratti et al., 2005; Jolly et al., 2005). In contrast, analyses of single species typically produce single (sometimes complex) haplotype networks even for geographically widespread species sampled on large spatial scales (Duran et al., 2004; Hurtado et al., 2004; Perrin et al., 2004; Waters et al., 2004a; Addison and Hart, 2005). Small mtDNA genetic distances between echinoderm individuals or clades may be an unreliable diagnosis for single biological species, especially if divergence is recent (Palumbi et al., 1997; Hart et al., 2003) or haplotypes are shared as a consequence of ancestral polymorphisms or hybridization (Addison and Hart, 2005). However, the large genetic distances found among P. exigua specimens are diagnostic for echinoderm species. Mitochondrial DNA sequence differences of 5%-7% among sea stars and other echinoderms have been found only among members of different species with identifiable morphological or reproductive differences and, in the absence of observed phenotypic differences, are interpreted as evidence of cryptic species diversity (Foltz, 1997; Hart et al., 1997; Lessios et al., 2001; O'Loughlin et al., 2003; Uthicke and Benzie, 2003; Waters and Roy, 2003; Uthicke et al., 2004; Waters et al., 2004a; Hart and Podolsky, 2005). If the Amsterdam Island and Cape Town haplotypes are members of the same species as Australian haplotypes, these would be the largest echinoderm intraspecific mtDNA genetic distances ever reported.
Our study does not definitively link the highly divergent haplotypes from African and island populations with the aboral gonopore phenotype (and some alternative mode of reproduction). So far, we lack mtDNA sequences from identified P. exigua populations with known aboral gonopores and conclusive data on gonopore locations for some of the non-Australian population samples that include highly divergent mtDNA haplotypes. Results of the mtDNA sequence data and network analysis suggest that the Durban and Port St. Johns specimens sampled by Waters and Roy (2004) had oral gonopores (this phenotype occurs in all three African localities sampled by Waters and Roy, 2004) and were conspecific with Australian P. exigua s. s. in their study and in Colgan et al. (2005). In addition, we conclude that the samples from Amsterdam Island and Cape Town may have included unnamed species with aboral gonopores. Thus, it appears that molecular and morphological data indicate the presence of multiple species within some African and island P. exigua populations, and we look forward to combined analyses of morphological, molecular, and reproductive variation across the broad range of this taxon.
Our discovery of cryptic species diversity within P. exigua still does not solve the most compelling puzzle of its biogeography: the very broad geographic distribution of the species without observed planktonic larval dispersal. As suggested by Fell (1962), the geographic distribution of this species may be partly explained by occasional rafting by small adults. Unfortunately, our understanding of this broad range and its biological causes appears to be complicated by the existence of a suite of cryptic species that probably includes more than one mode of development and dispersal, as recently discovered for other asterinid species (Dartnall et al., 2003; O'Loughlin et al., 2003). Altogether, the Indo-Pacific center of distribution and species richness for Parvulastra and other asterinids, plus the lack of haplotypes shared between Africa and Australia, suggest ancient dispersal of P. exigua out of the Indo-Pacific to African and island populations, with little recent gene flow between populations (Waters and Roy, 2004; Colgan et al., 2005). However, we need more comprehensive information on the geographic distributions of identified biological species before we can resolve the origin of Lamarck's little sea star.
We are supported by the Natural Sciences and Engineering Research Council of Canada, Simon Fraser University, and the Australian Research Council. We are grateful to the museum curators and assistants who provided access to specimens for analysis of gonopore distribution, especially A. Cabrinovic (London), C. Nielsen (Copenhagen), B. Hoeksema (Leiden), N. Ameziane and M. Eleaume (Paris), T. O'Hara (Melbourne), and D. Pawson (Washington, DC). Thanks to K. Dunbar, C. Griffiths, and M. Bruford for some unpublished observations on morphological variation and genetic diversity in asterinids from southern Africa, and to J. Waters for constructive comments on an earlier draft.
Addison, J. A., and M. W. Hart. 2005. Colonization, dispersal, and hybridization influence phylogeography of north Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59: 532-543.
Avise, J. 2004. Molecular Markers, Natural History, and Evolution, 2nd ed. Sinauer Associates, Sunderland, MA.
Balinsky, B. I. 1969. The echinoderms. Pp. 96-107 in A Natural History of Inhaca Island, Mocambique, W. Macnae and M. Kalk, eds. Witswatersrand University Press, Johannesburg, South Africa.
Baratti, M., E. Goti, and G. Messana. 2005. High level of genetic differentiation in the marine isopod Sphaeroma terebrans (Crustacea Isopoda Sphaeromatidae) as inferred by mitochondrial DNA analysis. J. Exp. Mar. Biol. Ecol. 315: 225-234.
Bright, K. M. F. 1938. The South African intertidal zone and its relation to ocean currents. 3. An area of the northern part of the West coast. Trans. R. Soc. S. Afr. 26: 67-88.
Bruguieres, J.-G. 1792. Encyclopedie Methodique, Histoire Naturelles des Poissons. Paris.
Byrne, M. 1992. Reproduction of sympatric populations of Patiriella species in New South Wales, asterinid seastars with direct development. Mar. Biol. 114: 297-316.
Byrne, M. 1995. Change in larval morphology in the evolution of benthic development by Patiriella exigua (Asteroidea: Asterinidae), a comparison with the larvae of Patiriella species with planktonic development. Biol. Bull. 188: 293-305.
Byrne, M. 2005. Viviparity in the sea star Cryptasterina hystera (Asterinidae)--conserved and modified features in reproduction and development. Biol. Bull. 208: 81-91.
Byrne, M., and A. Cerra. 1996. Evolution of intragonadal development in the diminutive asterinid sea stars Patiriella vivipara and P. parvivipara with an overview of development in the Asterinidae. Biol. Bull. 191: 17-26.
Byrne, M., A. Cerra, and J. T. Villinski. 1999. Oogenic strategies in the evolution of development in Patiriella (Asteroidea). Invertebr. Reprod. Dev. 36: 195-202.
Byrne, M., M. W. Hart, A. Cerra, and P. Cisternas. 2003. Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex. Biol. Bull. 205: 285-294.
Clark, A. M. 1974. Notes on some echinoderms of southern Africa. Bull. Br. Mus. (Nat. Hist.) Zool. 26: 421-487.
Clark, H. L. 1923. The echinoderm fauna of South Africa. Ann. S. Afr. Mus. 13: 221-435.
Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1660.
Colgan, D. J., M. Byrne, E. Rickard, and L. R. Castro. 2005. Limited nucleotide divergence over large spatial scales in the asterinid sea star Patiriella exigua. Mar. Biol. 146: 263-270.
Dartnall, A. J. 1971. Australian sea stars of the genus Patiriella (Asteroidea, Asterinidae). Proc. Linn. Soc. NSW 96: 39-51.
Dartnall A. J., M. Byrne, J. Collins, and M. W. Hart. 2003. A new viviparous species of asterinid (Echinodermata, Asteroidea, Asterinidae) and a new genus to accommodate the species of pan-tropical exiguoid sea stars. Zootaxa 359: 1-14.
Day, J. H. 1969. A Guide to Marine Life on South African Shores. Balkema, University of Cape Town, Cape Town, South Africa.
Day, J. H., and J. F. C. Morgans. 1956. The ecology of South African estuaries. 7. The biology of Durban Bay. Ann. Natal Mus. 13: 259-312.
Duran, S., C. Palacin, M. A. Becerro, X. Turon, and G. Giribet. 2004. Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol. Ecol. 13: 3317-3328.
Eyre, J. 1939. The South African intertidal zone and its relation to ocean currents. 7. An area in False Bay. Ann. Natal Mus. 9: 283-306.
Eyre, J., and T. A. Stephenson. 1938. The South African intertidal zone and its relation to ocean currents. 5. A sub-tropical Indian Ocean shore. Ann. Natal Mus. 9: 21-46.
Eyre, J., G. J. Broekhuysen, and M. I. Crichton. 1938. The South African intertidal zone and its relation to ocean currents. 6. The East London district. Ann. Natal Mus. 9: 83-111.
Fell, H. B. 1962. West-wind drift dispersal of echinoderms in the southern hemisphere. Nature 193: 759-761.
Foltz, D. W. 1997. Hybridization frequency is negatively correlated with divergence time of mitochondrial DNA haplotypes in a sea star (Leptasterias spp.) species complex. Evolution 51: 283-288.
Hart, M. W., M. Byrne, and M. J. Smith. 1997. Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51: 1848-1861.
Hart, M. W., M. Byrne, and S. L. Johnson. 2003. Patiriella pseudoexigua (Asteroidea: Asterinidae): a cryptic species complex revealed by molecular and embryological analyses. J. Mar. Biol. Assoc. UK 83: 1109-1116.
Hart, M. W., S. L. Johnson, J. A. Addison, and M. Byrne. 2004. Strong character incongruence and character choice in asterinid sea star phylogeny. Invertebr. Biol. 123: 343-356.
Hart, M. W., and R. D. Podolsky. 2005. Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars. Mol. Phylogenet. Evol. 34: 438-447.
Hunt, A. 1993. Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish Patiriella calcar and Patiriella exigua. Mar. Ecol. Prog. Ser. 92: 179-186.
Hurtado, L. A., R. A. Lutz, and R. C. Vrijenhoek. 2004. Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents. Mol. Ecol. 13: 2603-2615.
Johannesson, K. 1988. The paradox of Rockall: Why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar. Biol. 99: 507-513.
Jolly, M. T., D. Jollivet, F. Gentil, E. Thiebaut, and F. Viard. 2005. Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni along the north coast of France. Heredity 94: 23-32.
Kalk, M. 1958. Ecological studies on the shores of Mocambique. I. The fauna of intertidal rocks at Inhaca Island, Detagoa Bay. Ann. Natal Mus. 14: 189-242.
Knowlton, N. 1993. Sibling species in the sea. Annu. Rev. Ecol. Syst. 24: 189-216.
Knowlton, N. 2000. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420: 73-90.
Lamarck, J. B. P. A. 1816. Histoire Naturelle des Animaux Sans Vertebres. Verdiere, Paris.
Lee, T., and D. OFoighil. 2004. Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complex. Mol. Ecol. 13: 3527-3542.
Lessios, H. A., B. D. Kessing, and J. S. Pearse. 2001. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55: 955-975.
Linck, J. H. 1773. De Stellis Marinis Liber Singularis. Schuster. Leipzig.
Macnae, W. 1957. The ecology of the plants and animals in the intertidal regions of the Zwartkops estuary, near Port Elizabeth, South Africa, 2. J. Ecol. 45: 361-387.
Mallet, J. 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 10: 294-299.
Mikkelsen, P. M., and J. Cracraft. 2001. Marine biodiversity and the need for systematic inventories. Bull. Mar. Sci. 69: 525-534.
Mortensen, T. 1921. Studies of the Development and Larval Forms of Echinoderms. G. E. C. Gad, Copenhagen.
Mortensen, T. 1933. Papers from Dr. Th. Mortensen's Pacific Expedition 1914-18. LXVI. The echinoderms of St. Helena. (Other than crinoids). Vidensk. Medd. Dan. Nathist. Foren. 93: 401-473.
Munoz, J., A. M. Felicisimo, F. Cabezas, A. R. Burgaz, and I. Martinez. 2004. Wind as a long-distance dispersal vehicle in the Southern Hemisphere. Science 304: 1144-1147.
O'Loughlin, P. M. 2002. New genus and species of southern Australian and Pacific Asterinidae (Echinodermata, Asteroidea). Mem. Mus. Vic. 49: 277-296.
O'Loughlin, P. M., and J. M. Waters. 2004. A molecular and morphological revision of genera of Asterinidae (Echinodermata: Asteroidea). Mem. Mus. Vic. 61: 1-40.
O'Loughlin, P. M., J. M. Waters, and M. S. Roy. 2002. Description of a new species of Patiriella from New Zealand and review of Patiriella regularis (Echinodermata, Asteroidea) based on morphological and molecular data. J. R. Soc. NZ 32: 697-711.
O'Loughlin, P. M., J. M. Waters, and M. S. Roy. 2003. A molecular and morphological review of the asterinid Patiriella gunnii (Gray) (Echinodermata: Asteroidea). Mem. Mus. Vic. 60: 181-195.
Palumbi, S. R., G. Grabowsky, T. Duda, L. Geyer, and N. Tachino. 1997. Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51: 1506-1517.
Penrith, M. L., and B. F. Kensley. 1970. The constitution of the intertidal fauna of rocky shores of South West Africa. I. Luderitzbucht. Cimbebasia 1: 189-239.
Perrier, E. 1875. Revision de la collection de stellerides du Musee d'Histoire Naturelle de Paris. Arch. Zool. Exp. Gen. 4: 265-450.
Perrin, C., S. R. Wing, and M. S. Roy. 2004. Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fiords. Mol. Ecol. 13: 2183-2195.
Posada, D., and K. A. Crandall. 2001. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol. Evol. 16: 37-45.
Rowe, F. W. E., and J. Gates. 1995. Echinodermata. Zoological Catalogue of Australia, Vol. 33, A. Wells, ed. CSIRO, Melbourne.
Sites, J. W., Jr., and J. C. Marshall. 2004. Operational criteria for delimiting species. Annu. Rev. Ecol. Evol. Syst. 35: 199-227.
Stephenson, T. A. 1944. The constitution of the intertidal fauna and flora of South Africa. Ann. Natal Mus. 10: 261-358.
Stephenson, T. A., and A. Stephenson. 1972. Life Between Tidemarks on Rocky Shores. W. H. Freeman, San Francisco.
Stephenson, T. A., A. Stephenson, and C. H. Du Toit. 1937. The South African intertidal zone and its relation to ocean currents. 1. A temperate Indian Ocean shore. Trans. R. Soc. S. Afr. 24: 341-382.
Stephenson, T. A., A. Stephenson, and K. M. F. Bright. 1938. The South African intertidal zone and its relation to ocean currents. 4. The Port Elizabeth district. Ann. Natal Mus. 9: 1-19.
Stephenson, T. A., A. Stephenson, and J. H. Day. 1939. The South African intertidal zone and its relation to ocean currents. 8. Lambert's Bay and the West coast. Ann. Natal Mus. 9: 345-380.
Swofford, D. L. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sinauer Associates, Sunderland, MA.
Tarjuelo, I., D. Posada, K. A. Crandall, M. Pascual, and X. Turon. 2004. Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Mol. Ecol. 13: 3125-3136.
Templeton, A. R. 2001. Using phylogeographic analyses of gene trees to test species status and processes. Mol. Ecol. 10: 779-791.
Uthicke, S., and J. A. H. Benzie. 2003. Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific. Mol. Ecol. 12: 2635-2648.
Uthicke, S., T. D. O'Hara, and M. Byrne. 2004. Species composition and molecular phylogeny of the Indo-Pacific teatfish (Echinodermata: Holothuroidea) beche-de-mer fishery. Mar. Freshw. Res. 55: 837-848.
Verrill, A. E. 1913. Revision of the genera of starfishes of the subfamily Asterinidae. Am. J. Sci. 35: 477-485.
Villinski, J. T., J. L. Villinski, M. Byrne, and R. R. Raff. 2002. Convergent maternal provisioning and life history evolution in echinoderms. Evolution 56: 1764-1775.
Walenkamp, J. H. C. 1990. Systematics and zoogeography of Asteroidea (Echinodermata) from Inhaca Island, Mozambique. Zool. Verh. 261: 1-86.
Waters, J. M., and M. S. Roy. 2003. Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J. Biogeogr. 30: 1787-1796.
Waters, J. M., and M. S. Roy. 2004. Out of Africa: the slow train to Australasia. Syst. Biol. 53: 18-24.
Waters, J. M., P. M. O'Loughlin, and M. S. Roy. 2004a. Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Mol. Phylogenet. Evol. 32: 236-245.
Waters, J. M., P. M. O'Loughlin, and M. S. Roy. 2004b. Molecular systematics of some Indo-Pacific asterinids (Echinodermata, Asteroidea): does taxonomy reflect phylogeny? Mol. Phylogenet. Evol. 30: 872-878.
Whitelegge, T. 1889. Invertebrate fauna of Port Jackson. Subkingdom Echinodermata. Proc. R. Soc. NSW 23: 187-206.
Wiens, J. J., and T. A. Penkrot. 2002. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51: 69-91.
MICHAEL W. HART (1,*), CARSON C. KEEVER (1), ALAN J. DARTNALL (2), AND MARIA BYRNE (3)
(1) Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada; (2) School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland 4811, Australia; and (3) Department of Anatomy & Histology, F-13, University of Sydney, Sydney, New South Wales 2006, Australia
Received 2 May 2005; accepted 19 December 2005.
* To whom correspondence should be directed. E-mail: firstname.lastname@example.org
Table 1 Frequency of Parvulastra exigua specimens with gonopores on the oral or aboral surface in museum collections from St. Helena (Atlantic Ocean), southern Africa, Amsterdam/St. Paul/Kerguelen islands (Indian Ocean), and southern Australia Gonopores (b) Source (a) Collection locality Oral Aboral Uncertain MNHN 1493 Ruperts Bay, St. Helena 21 3 9 MNHN 841 St. Helena 44 5 NNM 5721 Ruperts Bay, St. Helena 7 NNM 5722 St. Helena, south coast 3 ZMUC Prosperous Bay, St. 1 Helena ZMUC Jamestown, St. Helena 1 USNM 1785 St. Helena 8 2 USNM E 8117 West Rocks, St. Helena 2 BMNH James Bay, St. Helena 5 1985.1.15 BMNH St., Helena 4 1954.10.28 MV F98060# St. Helena# 4# All St. Helena 84 19 16 collections MNHN 1492 Baiia de Massamides, 1 Angola MNHN 3894 Cape of Good Hope 2 ZMUC Isipingo, Natal 6 ZMUC Algoa Bay, South Africa 4 ZMUC Table Bay, South Africa 1 BMNH False Bay, South Africa 2 1898.1.11 BMNH Cape of Good 3 1904.4.20 Hope station 176 BMNH Saldanha Bay, 1 1948.3.16 South Africa BMNH Port Elizabeth, 3 1891.7.9. South Africa MV F 98061# Durban, South Africa# 3# 1# MV F98062# Cape Town, South 3# 1# Africa# All southern Africa 23 6 2 collections MNHN 2128 St. Paul Island 8 12 MNHN 2202 St. Paul 6 7 MNHN 3925 St. Paul 4 48 24 MNHN 3926 St. Paul 5 13 BMNH St. Paul 5 1975.12.4 BMNH St. Paul station 8a 3 1975.12.4 BMNH Amsterdam Island (all) (c) 1975.12.4 MV F 98063# Amsterdam Island# 2# MNHN 1568 Kerguelen Island 2 2 All Indian Ocean 33 48 60 collections MNHN 2355 Sydney, Australia 12 MNHN 2443 Port Jackson, Australia 4 All Australia 16 collections TOTAL 146 73 74 Italic type indicates accessions for which mtDNA sequence data were available. (a) All specimens came from collections of the Musee Nationale d'Histoire Naturelle (MNHN); Nationaal Natuurhistorisch Museum (NNM); Zoological Museum, University of Copenhagen (ZMUC); British Museum (BMNH); National Museum of Natural History (USNM); and Museum Victoria (MV). (b) Oral gonopores, on the surface of the body disk next to the mouth (Fig. 1A), are associated with deposition of egg masses in P. exigua and other asterinid species; aboral gonopores (Fig. 1B) are found in all other species with broadcast spawning of gametes or internal fertilization and intragonadal brooding of juveniles. Only conclusively identified states are noted; cases in which the location of the gonopores could not be clearly ascertained due to poor preservation of the specimen were scored as "uncertain." (c) This sample included large specimens (probably adults) with oral gonopores and a size series of individuals (probably juveniles) in which gonopore location could not be determined; specimens from this sample are not included in column totals. Note: Accessions for which mtDNA sequence data were available indicated with #.
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|Author:||Hart, Michael W.; Keever, Carson C.; Dartnall, Alan J.; Byrne, Maria|
|Publication:||The Biological Bulletin|
|Date:||Apr 1, 2006|
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