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Biogeography of Asterias: North Atlantic Climate Change and Speciation

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Biogeography of Asterias: North Atlantic Climate Change and Speciation Reference: Biol. Bull. 201: 95–103. (August 2001) Biogeography of Asterias: North Atlantic Climate Change and Speciation JOHN P. WARES Duke University Zoology, Box 90325, Durham, North Carolina 27708 Abstract. Fossil evidence suggests that the seastar genus 1983; Vermeij, 1991). Today, two species are recognized in Asterias arrived in the North Atlantic during the trans- the North Atlantic: A. forbesi on the North American coast, Arctic interchange around 3.5 Ma. Previous genetic and primarily from Cape Hatteras to Cape Cod (Franz et al., morphological studies of the two species found in the At- 1981), and A. rubens on the American coast primarily from lantic today suggested two possible scenarios for the spe- Cape Cod northward (Franz et al., 1981), and on the Euro- ciation of A. rubens and A. forbesi. Through phylogenetic pean coast from Iceland to western France (Clark and and population genetic analysis of data from a portion of the Downey, 1992; Hayward and Ryland, 1995). American cytochrome oxidase I mitochondrial gene and a fragment of populations of A. rubens have been previously described as the ribosomal internal transcribed spacer region, I show that A. vulgaris, a junior synonymy (Clark and Downey, 1992). the formation of the Labrador Current 3.0 Ma was probably These species co-occur over a broad range of the North responsible for the initial vicariance of North Atlantic As- American continental shelf centered on Cape Cod (Gosner, terias populations. Subsequent adaptive evolution in A. 1978; Menge, 1979; Franz et al., 1981). forbesi was then possible in isolation from the European Two current hypotheses attempt to explain the recent species A. rubens. The contact zone between these two speciation between A. forbesi and A. rubens. Schopf and species formed recently, possibly due to a Holocene found- Murphy (1973) suggested that they were a germinate spe- ing event of A. rubens in New England and the Canadian cies pair formed by a late Pleistocene (0.02–2.5 Ma) vicari- Maritimes. ance event (i.e., a separation of populations) at Cape Cod, possibly due to lower sea levels during glacial maxima. Introduction There is some evidence for hybridization between these The North Atlantic Ocean is populated by hundreds of seastars, but the separation could be maintained by localized taxa which invaded from the North Pacific following the adaptation to the different thermal regimes north and south opening of the Bering Strait about 3.5 million years ago of Cape Cod (Franz et al., 1981). However, this thermal (Ma; Durham and MacNeil, 1967; Vermeij, 1991). Some of boundary was latitudinally unstable throughout the Pleisto- these species have maintained genetic contact with source cene (Cronin, 1988) and only in the past 20,000 years populations in the Pacific until recently (Palumbi and Kess- (Holocene) has it returned to its current state. If the geo- ing, 1991; van Oppen et al., 1995), but many of them have graphical isolation between these taxa was recent, as pro- subsequently differentiated from the source populations and posed in Schopf and Murphy (1973), then strong natural are now recognized as distinct species (e.g., Gosling, 1992; selection within each region has prevented widespread hy- Reid et al., 1996; Collins et al., 1996). Circumstantial bridization. evidence suggests strongly that the seastar genus Asterias The second hypothesis, based on morphological and pa- (Echinodermata: Asteroidea: Asteriidae: Asteriinae) partic- leoceanographic evidence, suggested a late Pliocene (ap- ipated in the trans-Arctic interchange (Worley and Franz, proximately 2.5–5 Ma) separation of Asterias into distinct North American and European species, followed by a Ho- locene recolonization of North America by the European Received 28 September 2000; accepted 10 May 2001. Current address: Dept. of Biology, University of New Mexico, Castetter species A. rubens (Worley and Franz, 1983). This hypoth- Hall, Albuquerque, NM 87131. E-mail: [email protected] esis would therefore suggest that the differentiation between 95 96 J. P. WARES Table 1 were stored at Ϫ80°C. PCR amplification of an approxi- Collection sites for individuals of each species in this study mately 700-bp portion of the mitochondrial cytochrome c oxidase I (COI) protein-encoding gene was performed using Species [Population] Location Sample size the primers LCO1490 and HCO 2198 from Folmer et al. (1994). Amplification was performed in 50-␮l reactions A. rubens [North America] Maine (44°N, 69°W) 12 containing 10–100 ng DNA, 0.02 mM each primer, 5 ␮l Nova Scotia (46°N, 62°W) 6 Newfoundland (50°N, 55°W) 5 Promega 10ϫ polymerase buffer, 0.8 mM dNTPs (Pharma- A. rubens [Europe] Iceland (64°N, 22°W) 2 cia Biotech), and 1 unit Taq polymerase (Promega). Reac- Norway (63°N, 10°E) 8 tions took place in a Perkin-Elmer 480 thermal cycler with Ireland (53°N, 10°E) 10 a cycling profile of 94° (60 s) Ϫ40° (90 s) Ϫ72° (150 s) for France (48°N, 3°E) 5 40 cycles. The internal transcribed spacer (ITS) region was A. forbesi North Carolina (34°N, 76°W) 5 Cape Cod (41°N, 70°W) 3 amplified under similar conditions, with an annealing tem- A. amurensis Sea of Japan (43°N, 131°E) 4 perature of 50°C and with primers ITS4 and ITS5 (White et Leptasterias sp. Iceland (64°N, 22°W) 1 al., 1990). For each individual, sequences were obtained for three to four clones, and the consensus sequence was ob- Voucher specimens are being maintained in the marine invertebrate collections of C. W. Cunningham at Duke University. tained to eliminate Taq error. PCR products were prepared for sequencing and were cycle-sequenced as in Wares (2001) using both PCR prim- the two Atlantic species is entirely due to long-term isola- ers. COI sequences representing each individual in this tion. Thus, subsequent physiological adaptations to warmer study have been deposited with GenBank (AF240022- water in A. forbesi (Franz et al., 1981) are independent of 240081); ITS sequences were only obtained for 10 individ- the speciation event. Essentially, the distinction between uals, representing each species and region, and are also these species reflects either primary divergence due to se- accessible in GenBank (AF346608-AF346617). Sequences lection or secondary contact following vicariance (Endler, were aligned and edited for ambiguities using complemen- 1977). tary fragments in Sequencher 3.0 (Genecodes Corp., Cam- In this study, mitochondrial and nuclear sequence data bridge, MA). No gaps or poorly aligned regions occurred in were collected from populations of A. forbesi and A. rubens the COI alignment, but missing characters were trimmed throughout North America and Europe, as well as from from the ends of the alignment to produce equal sequence populations of the Pacific sister taxon A. amurensis (Clark lengths for all individuals. In the ITS alignment, all missing and Downey, 1992). Phylogenetic and population genetic or ambiguous characters, including gaps, were removed. assays were used to test the hypotheses described above. It Consensus sequences were exported as a NEXUS file for appears that Worley and Franz (1983) were remarkably subsequent analysis in PAUP*4.0b4a (Swofford, 1998). accurate in suggesting a Pliocene speciation followed by a recent invasion of A. rubens from Europe, even in their Phylogenetic analysis prediction of details of timing, mechanisms, and effects. Although selection may have driven some of the diver- A heuristic search for the set of most-parsimonious trees gence, it now seems clear that the initial separation of A. based on the COI data was performed using PAUP*4.0b4a rubens and A. forbesi is due to late Pliocene changes in (Swofford, 1998). Trees were rooted using Leptasterias climate and ocean current flow, whereas North American polaris (Asteriinae) and individuals of A. amurensis. Start- populations of A. rubens are very recent arrivals. ing trees were obtained via stepwise addition, with simple addition sequence. Tree-bisection-reconnection was used Materials and Methods for branch swapping, and branches were collapsed if the maximum branch length was zero. Asterias specimens were collected from intertidal sites Maximum-likelihood (ML) phylogenies were also gener- listed in Table 1. Tube feet were immediately placed in 95% ated in PAUP*. The best-fit model for all likelihood anal- ethanol or DMSO buffer (0.25 M EDTA pH 8.0, 20% yses (HKY with ⌫-distributed rate variation; Hasegawa et DMSO, saturated NaCl; Seutin et al., 1991). Species were al., 1985; Yang, 1994) was determined by adding parame- identified on the basis of key morphological characters ters until the likelihood description of the neighbor-joining described in Clark and Downey (1992) and Hayward and tree did not significantly improve (Goldman, 1993; Cun- Ryland (1995). ningham et al., 1998), using the likelihood-ratio test of ModelTest (Posada and Crandall, 1998). A series of boot- DNA extraction and amplification strap replicates (100 ML replicates, heuristic search) using DNA was phenol-extracted from each specimen follow- PAUP* were performed to determine support for interspe- ing the protocol in Hillis et al. (1996). These extractions cific relationships in the clade. Estimates of the transition- BIOGEOGRAPHY OF ASTERIAS 97 transversion ratio for the HKY model, along with the other possible rooted trees was calculated using 107 simu- gamma-distributed parameter for among-site rate heteroge- lations in GeneTree. neity, were held constant for bootstrap replicates. A maxi- mum likelihood phylogeny of the ITS sequence data was Tests of rate constancy also generated using the appropriate best-fit model (F81: Likelihood-ratio tests (Felsenstein, 1988; Goldman, equal rates among sites, unequal base frequencies). 1993) were used to test the hypothesis that the data collected Estimates of speciation time within the North Atlantic were consistent with a constant-rate Poisson-distributed require an estimate of the mutation rate (␮).
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