© 2000 by The Society for Integrative and Comparative Biology
Phylogenetic Analysis of Molecular Lineages in a Species-Rich Subgenus of Sea Stars (Leptasterias Subgenus Hexasterias)1
1 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803-1715
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Among diverse marine invertebrate taxa, the evolution of a non-planktotrophic larva is often associated with increased rates of cladogenesis, compared to related taxa that retain the ancestral planktotrophic larval form. Molecular phylogenetic analyses of non-planktotrophic (and, presumably species-rich) clades of marine invertebrates are rare. Here we analyze 1542 base pairs of mitochondrial DNA sequence comprising two gene regions, the cytochrome oxidase I gene and the putative control region and flanking sequences, for 23 molecular lineages in the obligately brood-protecting asteroid genus Leptasterias. Using maximum likelihood, minimum evolution, and maximum parsimony methods, five major clades were identified that corresponded to five taxa (species or species complexes) in the subgenus Hexasterias, section camtschatica (following the taxonomy of Walter K. Fisher). Two clades (L. aequalis> complex and L. aleutica/L. camtschatica complex) were composed of numerous molecular lineages (7–8 lineages/clade), and several clades had multiple shallow nodes, suggestive of recent radiations. Two of the clades (L. aleutica/L. camtschatica complex and L. hexactis complex), with geographic ranges restricted to latitudes higher than 48°N, were lacking deep phylogenetic nodes. This pattern is consistent with the hypothesis that high-latitude taxa have high rates of extinction due to repeated climatic crises. A log-likelihood ratio test performed on the camtschatica section, including a member (Leptasterias polaris) of the polaris section and using a representative (L. mülleri) of Leptasterias subgenus Leptasterias as an outgroup, demonstrated that the camtschatica section is monophyletic.
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INTRODUCTION |
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The mode of reproduction and the evolution of a non-planktotrophic larva in marine invertebrates potentially influence many micro- and macro-evolutionary processes, including dispersal and inbreeding levels (see Knowlton and Jackson, 1993
), possibility of local adaptation (e.g., Behrens Yamada, 1989), fecundity and recruitment (see Strathmann, 1985, 1990), geographic range (e.g., Emlet, 1995), rates of extinction (see Poulin and Féral, 1996) and rates and mode of speciation (e.g., Pearse and Bosch, 1994; Poulin and Féral, 1994). One non-planktotrophic larval type that has evolved repeatedly among echinoderms is the brooded lecithotrophic form (McEdward and Janies, 1993, 1997). This larval form occurs in all asteroid orders and most families and is often the predominant mode of reproduction in high-latitude echinoderm taxa in both hemispheres (Emlet et al., 1987; Emlet, 1990). For example, the forcipulate family Asteriidae includes at least one subarctic (Leptasterias) and two Antarctic (Anasterias, Lysasterias) genera that are both obligate brooders and very species-rich. However, our knowledge of the evolutionary significance of these patterns is severely impeded by a lack of information about mode of reproduction, phylogenetic relationships and even basic taxonomy of the various groups.
Some of these difficulties are illustrated by the six-rayed sea stars of the genus Leptasterias, subgenus Hexasterias. The taxonomic and morphological complexity of this group has been recognized for most of the 20th century (e.g., Verrill, 1909, 1914). The most recent taxonomic revision (Fisher, 1930) recognized two sections (polaris and camtschatica) within the subgenus Hexasterias, with two and eight nominal species, respectively. Most of these nominal species included many described forms and subspecies, but more recent taxonomic treatments of the six-rayed Leptasterias along the North American Pacific coast (e.g., Lambert, 1981) have reduced the number of described species to one or a few, following the work of Chia (1966).
About a decade ago, we (Kwast et al., 1990; Stickle et al., 1992; Foltz and Stickle, 1994) began a study of the allozyme genetics and taxonomy of the subgenus Hexasterias. Our initial work focused on the nominal species L. aequalis, L. hexactis and L. pusilla, which are generally believed to be the most abundant species in the subgenus along the North American Pacific coast from central California to southern Alaska. More recently, we have employed additional molecular techniques, primarily restriction fragment length polymorphisms in PCR-amplified mitochondrial DNA (mtDNA PCR-RFLPs) and direct sequencing of mtDNA (see recent review by Foltz, 1998). We have also expanded the survey to include additional samples from the Aleutian Islands, which are reported here for the first time.
Previous work resulted in the identification of 11 mtDNA molecular lineages (referred to as haplotypes and lettered A through K), that were mostly genetically differentiated (Nei's unbiased allozyme distances between 0.09–0.20; Foltz et al., 1996a) and reproductively isolated from each other (frequency of hybridization between sympatric haplotypes less than 1.3%; Foltz, 1997). These results are consistent with most of the 11 previously-identified haplotypes representing separate species. Amounts of allozyme differentiation (Foltz et al., 1996a), sequence distance (Hrincevich and Foltz, 1996) and morphological divergence (Foltz et al., 1996b) among haplotypes were all low, suggesting either a recent radiation of haplotypes or a slow rate of evolution for both nuclear and mitochondrial genes.
The present report was stimulated in part by a lack of resolution of the position of certain lineages in our earlier phylogenetic analysis (Hrincevich and Foltz, 1996). By sampling additional haplotypes and sequencing a second mtDNA gene region, our goal was to provide a better-supported phylogeny that would answer some questions, such as whether or not the camtschatica section of the subgenus Hexasterias is monophyletic, that were not addressed in the earlier reports. We were also interested in comparing our phylogenetic results with the recent taxonomic reassessment of the camtschatica section by Flowers (1999).
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MATERIALS AND METHODS |
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Samples
Approximately half of the samples included in this study (Table 1) were selected from earlier studies of mtDNA PCR-RFLPs (Foltz et al., 1996a
, b; Foltz, 1998). The remainder were from sea stars collected in the summer of 1997 in the Aleutian Islands. Genomic DNA was extracted as in Foltz et al. (1996a). A representative of each haplotype A through X that had been identified in the PCR-RFLP survey was sequenced for approximately two-thirds of the mitochondrial cytochrome oxidase I (COI) gene and for about 550 base pairs (bp) of a PCR product representing the mtDNA putative control region and flanking sequences (henceforth called CR; see Foltz et al., 1996b, their Fig. 2). No COI sequence was obtained from haplotype M, which will not be considered further in this paper. The 23 remaining haplotypes can be assigned to Fisher's camtschatica section based on morphological criteria (Flowers, 1999).
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Primer design, PCR amplification and sequencing
Amplification of the CR region was carried out using the 12Sa/16Sa primers of Smith et al. (1993
), which are located at positions 6818 and 7569, respectively. All positions refer to the location of the 5' end of the primer relative to the Asterina pectinifera complete mtDNA sequence (Asakawa et al., 1995). These primers correspond to highly conserved regions among echinoderms at the 3' ends of the two mitochondrial rRNA genes and jointly amplify about 620 bp in Leptasterias. Initial amplification of about 2.4 Kb of mtDNA containing the entire COI gene and flanking sequences was carried out using the unnamed PCR primers of Hart et al. (1997), located at positions 11725 or 14098. We designed 4 internal primers for sequencing, by comparing orthologous echinoderm COI gene sequences from 17 asteroids, 16 holothuroids and 2 echinoids. From this search, two primers, INOECH-1 and INOECH-3, were designed which would jointly amplify about 700-bp. Two additional Hexasterias-specific nested primers, LEPint-F and LEPint-R, were designed to extend our final COI sequences to 993-bp, when used in combination with the Hart et al. (1997) primers. The sequences of the four primers reported here (using standard IUPAC codes) are as follows:
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Double-stranded PCR amplifications and manual sequencing were carried out as in Hrincevich and Foltz (1996). Automated cycle sequencing was also performed, using Applied BioSystems ABI-Prism Dye-Terminator reactions (Perkin-Elmer, Norwalk, Conn.), as described in Rocha-Olivares et al. (1999).
Sequence alignment and phylogenetic analysis
Sequences were initially aligned using ClustalW v. 1.7 (Thompson et al., 1994). All COI sequences were 993 bp long without insertion/deletions (indels), whereas the CR sequences varied in length from 541 bp to 546 bp due to hypothesized indels within the putative control region. We adjusted the ClustalW alignment by eye to maximize the number of phylogenetically informative sites, resulting in a 549-bp alignment for the CR sequences.
Phylogenetic analyses were carried out with the program PAUP* v4.0b1 (Swofford, 1998). Maximum parsimony (MP, Sober, 1983) was implemented using the branch-and-bound algorithm to determine phylogenetic relationships among the camtschatica section haplotypes. Clade support was assessed from similar reconstructions performed on 500 replicate data sets obtained through nonparametric bootstrapping. In order to determine the degree to which tree topology depended on the method of phylogenetic reconstruction, we performed both maximum likelihood (ML, Felsenstein, 1981) and distance-based searches, assuming the parameter-rich model of evolution proposed by Hasegawa, Kishino, and Yano (HKY85, Hasegawa et al., 1985), which allows for different rates of evolution for transitions and transversions and for unequal base frequencies. We calculated the ML estimates of the transition/transversion bias parameter 
and the shape parameter 
of the gamma distribution, assumed to represent the distribution of evolutionary rates among sites (Yang, 1993). The distance-based method used was minimum evolution (ME, Rzhetsky and Nei, 1992), implemented using a matrix of pair-wise genetic distances calculated by ML assuming the HKY85 model of evolution and the same parameters obtained in the ML search. Five hundred replicate data sets obtained through nonparametric bootstrap were used to assess branch support in the ME reconstruction. These trees were rooted by outgroup on orthologous sequences of Leptasterias polaris (subgenus Hexasterias, section polaris) collected from Glacier Bay, Alaska (Table 1).
The null hypothesis (H0) of monophyly of the camtschatica section was tested using a log-likelihood ratio test (L-LRT, Huelsenbeck et al., 1996). For this test, we included orthologous sequence data from Leptasterias mülleri, a five-rayed sea star (subgenus Leptasterias) collected from Iceland (Table 1). Two ML searches were performed under the HKY85 model of evolution: one unconstrained and another one in which non-monophyly of the camtschatica section was enforced. In order to determine the significance of the test statistic (
= 2[ln L1 – ln L0]; where L0 = maximized likelihood under the H0 of monophyly and L1 = maximized likelihood under the hypothesis of non-monophyly), a null distribution of was constructed via Monte Carlo simulations. One hundred data sets of the same size as the original were generated with the program Seq-Gen v1.1 (Rambaut and Grassly, 1997) using the ML tree and parameters obtained under the H0. A nonparametric bootstrap analysis consisting of unconstrained searches of 500 pseudo-replicates was conducted on this data matrix using MP as the optimality criterion.
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RESULTS |
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We identified 24 PCR-RFLP haplotypes among ca. 1,650 six-rayed sea stars examined (Table 2), and assigned them arbitrary letter designations A–X. Haplotypes L–X had not been previously reported. After alignment, the sequence data consisted of 993 bp of the COI gene and 549 bp of the CR region for 23 haplotypes (A–X excluding M, see Table 1) plus Leptasterias polaris and Leptasterias mülleri as outgroups. The complete sequence alignment for each gene region has been deposited with GenBank and is also available from the authors upon request. For the camtschatica section plus L. polaris, of the 1,542 total aligned sites, 268 sites were variable, of which 168 were parsimony informative.
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The most parsimonious reconstructions consisted of 24 trees (466 steps, CI = 0.69, RI = 0.83). All haplotypes except J were grouped in one of two clades with high bootstrap support (above 90%, Fig. 1A). Conflicting relationships among the most parsimonious trees resulted in polytomies in the strict consensus tree (Fig. 1A) and involved haplotypes C, G and W in one clade, and haplotypes N, Q, S, and T, in the second. Most of the other branches in the MP tree were well supported, with bootstrap values above 90% (Fig. 1A). High levels of congruence among the different methods of phylogenetic reconstruction indicated that the phylogenetic signal in the data set was robust to the different assumptions of each method. The ML reconstruction (–ln L = 4,701.02, transition/transversion ratio = 3.11,
= 0.101) recovered essentially the same topology as MP, in which the regions of conflict or poor bootstrap support were resolved but characterized by short branch lengths (Fig. 1B). The same observation was true for the ME tree (score = 0.415), where the observed topological differences were mostly limited to those relationships that were consistently poorly supported by the bootstrap analysis (Figs. 1A and 1C).
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The most parsimonious (MP) and most likely (ML) unconstrained searches carried out including a representative of Leptasterias mülleri produced trees in which the camtschatica section was monophyletic and supported in 68% of the bootstrap pseudo-replicates (not shown). The topological differences between the MP and ML trees could be mostly predicted from the results obtained with the abridged data set without Leptasterias mülleri (Figs. 1A and 1B)—namely the polytomies involving haplotypes C, G and W, on one hand, and haplotypes N, Q, S, and T, on the other. The
null distribution constructed from the Monte Carlo simulations produced a highly skewed distribution with ca. 54% of the simulations with < 2.7. Therefore, the null hypothesis of monophyly of the camtschatica section could not be rejected ( = 2.70, P > 0.46, Table 3).
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DISCUSSION |
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Comparison of molecular and morphological characters between our PCR-RFLP haplotypes A–X and museum voucher specimens has revealed that the five clades of molecular lineages identified here can be associated with one or more of the nominal species that were placed by Fisher (1930)
in the camtschatica section of the subgenus Hexasterias (Flowers, 1999): haplotype J corresponds to L. leptodoma; haplotypes E, F, H and P correspond to L. alaskensis; haplotypes A, B, D, K, L, V and X correspond to L. aequalis; haplotypes C, G and W correspond to L. hexactis; and haplotypes I, N, O, Q, R, S, T and U correspond to L. aleutica/L. camtschatica. In the discussion below, we will refer to these five groups as "major clades." In Tables 1 and 2, each of the five clades (except L. leptodoma) is called a "complex," because of the possibility of unrecognized taxonomic heterogeneity. Compared to our previous analysis (Hrincevich and Foltz, 1996), the current phylogeny was better resolved, particularly concerning the position of L. leptodoma. This species was consistently basal to the remaining camtschatica section haplotypes (Fig. 1), whereas earlier we had been unable to determine its position with any confidence. The inclusion of additional PCR-RFLP haplotypes and the use of two different mtDNA regions resolved most of the evolutionary relationships among the haplotypes. Lack of resolution observed in reconstructions points to recent radiations occurring within two of the remaining four major clades. Otherwise, the rest of the phylogenetic relationships were clearly resolved and well supported, judging from the high bootstrap support values and from the congruent topologies of trees obtained with various methods of phylogenetic reconstruction.
The existence of multiple lineages within four of the major clades is consistent with suggestions that a non-planktotrophic larval form is associated with a high rate of cladogenesis (Pearse and Bosch, 1994; Poulin and Féral, 1994). This observation is tempered by the lack of comparable data on molecular lineages for closely-related Asteriid taxa with planktotrophic larvae, such as exists, for example, in the gastropod genus Littorina (Reid, 1990; Reid et al., 1996). Also, we do not have allozymic or other nuclear-encoded genotypes for many of the sympatric haplotypes involved in the apparent recent radiations (mostly L through X). That information is required to test whether the lineages represent separate species or within-species polymorphisms. Some insights into the scarcity of deep nodes in the L. hexactis and L. aleutica/L. camtschatica clades (compared to the abundance of deep nodes in the equally lineage-rich L. aequalis clade) can be gained from the observation that, in both of these high-latitude clades, most of the haplotypes are found only in a restricted number of locations. In the L. hexactis clade, haplotypes G and C are largely restricted to the Lynn Canal region of Alaska and the Puget Sound, respectively, and only haplotype W is broadly distributed (from Kodiak Island, Alaska, to Wolf Island, British Columbia). Similarly, in L. aleutica/L. camtschatica, most of the eight haplotypes have so far been found at only three islands in the central Aleutians (Kiska, Amchitka and Kanaga). However, haplotype T has also been collected at Unalaska Island and, based on morphological criteria, the L. aleutica/L. camtschatica clade occurs throughout the Aleutian Islands and much of the northwestern Pacific Ocean (Fisher, 1930). Given that the Aleutian Islands have been repeatedly covered by ice sheets during the last million years (e.g., Pielou, 1991), the more northerly-distributed lineages probably have had a greater probability of extinction than did their southern counterparts in the L. aequalis clade. Assuming (based on the discussion in Hart et al., 1997) a rate of COI sequence divergence of 1.4%–5% per million years (My) and excluding haplotype O, which occurred only once in our samples, the nodes in the L. hexactis and L. aleutica/L. camtschatica clades date to between 40,000 and 500,000 years ago, compared to a range of 80,000–2.3 My ago in L. aequalis. These estimated dates are consistent with the suggestion that separation and compression of geographic ranges caused by glacial advances during the Pleistocene are responsible for some or all of the lineage splitting events in the more northerly-distributed major clades. The situation in L. alaskensis is intermediate to the above extremes in both estimated time of lineage splitting (range, 100,000–1.4 My ago) and geographic range, with haplotypes E, H and P largely restricted to Amchitka and Shemya Islands, and only haplotype F having a broad distribution (from Shemya, Alaska to Wolf Island, British Columbia). The situation in the L. hexactis and L. aleutica/L. camtschatica clades corresponds to the model of Poulin and Féral (1996), in which low-dispersal clades have higher rates of speciation than do high-dispersal clades, with a "climatic crisis" resulting in a loss of most deep nodes among extant lineages that inhabit higher latitudes.
Whether these conclusions about rates and patterns of cladogenesis and extinction in high-latitude taxa of Leptasterias can be generalized to other marine invertebrate species, particularly those with different life histories, can only be determined by additional research. Available data, though, make it unlikely that a "climatic crisis" scenario would apply with equal force to species that are restricted to the sublittoral zone or to lower latitudes. Lindberg and Lipps (1996), for example, suggested that there was little evidence of high rates of either speciation or extinction during the Pleistocene for temperate (i.e., southern Californian) rocky shore invertebrate taxa, possibly because of the brief duration of potential isolating events. They did acknowledge that the fossil record provides little evidence on rates of molecular divergence that precedes morphological differentiation, which is the subject of the present work. Similarly, Vermeij (1989) reported that geographical restriction (a surrogate measure of extinction) in Northwest-Pacific molluscs was higher in intertidal and shallow sublittoral taxa than in those with a deeper or broader tidal zone distribution.
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ACKNOWLEDGMENTS |
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For help with field collection we thank Guiseppe Bucciarelli, Jeff Coleman, James Estes, Jared Figurski, John L. Guerin, Masaya Katoh, Kurt E. Kwast, John S. Pearse, Vicki Pearse, Stanley D. Rice, Shane K. Sarver, Thomas Schulz, Thomas C. Shirley, William B. Stickle, and Jeffrey W. Tamplin. Laboratory and technical assistance was provided by Michael T. Bolton, Ronald Bouchard, Jeryl P. Breaux, Erica L. Campagnaro, Mary M. Coenen, Nanette Crochet, Donna L. Dittmann, Scott W. Herke, Amy E. Himel, Brian Kansas, Jeffrey J. LaFleur, Adriane R. Marchand, and Deborah Taranik. Jonathan M. Flowers, Scott W. Herke, Dorothy P. Prowell and two anonymous reviewers made helpful comments on earlier drafts of the manuscript. John P. Wares provided DNA and morphological identification for the sample of Leptasterias mülleri from Iceland. This research was supported by grants from the National Science Foundation and the Louisiana Board of Regents (D. W. Foltz, co-P.I.). Some of the collecting trips were funded by a grant from the National Geographic Society to W. B. Stickle.
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FOOTNOTES |
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1 From the Symposium Evolution of Starfishes: Morphology, Molecules, Development, and Paleobiology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 6–10 January 1999, at Denver, Colorado.
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