Life-history predicts past and present population connectivity in two sympatric sea stars

Abstract

Life-history traits, especially the mode and duration of larval development, are expected to strongly influence the population connectivity and phylogeography of marine species. Comparative analysis of sympatric, closely related species with differing life histories provides the opportunity to specifically investigate these mechanisms of evolution but have been equivocal in this regard. Here, we sample two sympatric sea stars across the same geographic range in temperate waters of Australia. Using a combination of mitochondrial DNA sequences, nuclear DNA sequences, and microsatellite genotypes, we show that the benthic-developing sea star, Parvulastra exigua, has lower levels of within- and among-population genetic diversity, more inferred genetic clusters, and higher levels of hierarchical and pairwise population structure than Meridiastra calcar, a species with planktonic development. While both species have populations that have diverged since the middle of the second glacial period of the Pleistocene, most P. exigua populations have origins after the last glacial maxima (LGM), whereas most M. calcar populations diverged long before the LGM. Our results indicate that phylogenetic patterns of these two species are consistent with predicted dispersal abilities; the benthic-developing P. exigua shows a pattern of extirpation during the LGM with subsequent recolonization, whereas the planktonic-developing M. calcar shows a pattern of persistence and isolation during the LGM with subsequent post-Pleistocene introgression.

Keywords: gene flow; phylogeography; population genetics; population structure.

Figure 1

Map of Australia with major currents and biogeographic provinces. Note that Tasmania was only partially glaciated during the Pleistocene with glaciers restricted to high elevation plateaus

Figure 2

Map of sampling locations and mtDNA haplotype networks. Parvulastra exigua on top and Meridiastra calcar on the bottom. Networks are colored by region identically to the sampling sites on the maps, and branch lengths are proportional to genetic distance among haplotypes. Scale bars on the bottom right of each network image represent one mutational change. Abbreviations and regions are defined in Table 1

Figure 3

Bayesian clustering results for Parvulastra exigua. Top six panels are spatial interpolations of the six genetic clusters detected by TESS. The bottom panel are the K = 6 results from STRUCTURE plotted at the population level

Figure 4

Bayesian clustering results for Meridiastra calcar. Top six panels are spatial interpolations of the four genetic clusters detected by TESS. The bottom panel are the K = 3 results from STRUCTURE plotted at the population level

Figure 5

Visual representation of mtDNA pairwise ϕ_ST values for P. exigua (top panel) and M. calcar (bottom panel)

Figure 6

Population divergence time estimates for both species. Population tree used for each coalescent analysis is represented in the upper right corner. (a) Parvulastra exigua—Only samples that had no missing data across the five nDNA loci and mtDNA locus were included and samples within northern NSW (AB, PS1; labeled as AB), within central NSW (DY, LB, BM; labeled as NSW), within southern NSW (SH1, SH2; labeled as SH), and within SA (WA, TK; labeled as SA) were combined and randomly subsampled into representative populations. (b) Meridiastra calcar—Samples from within northern and central NSW (AB, PS1, DY, LB, BM; labeled as NSW), within southern NSW (SH1, SH2; labeled as SH), within eastern TAS (FB, PB; labeled as FBPB), within western TAS (PS, ROB; labeled as PSROB), and within WA (WCB, WCA; labeled as SA) were combined