Phylogeography of the Pantropical Sea Urchin Tripneustes: Contrasting Patterns of Population Structure Between Oceans

Abstract

Abstract. To understand how allopatric speciation proceeds, we need information on barriers to gene flow, their antiquity, and their efficacy. For marine organisms with planktonic larvae, much of this information can only be obtained through the determination of divergence between populations. We evaluated the importance of ocean barriers by studying the mitochondrial DNA phylogeography of Tripneustes, a pantropical genus of shallow water sea urchin. A region of cytochrome oxidase I (COI) was sequenced in 187 individuals from locations around the globe. The COI phylogeny agreed with a previously published phylogeny of bindin that barriers important to the evolution of Tripneustes are: (1) the cold water upwelling close to the tip of South Africa, (2) the Isthmus of Panama, (3) the long stretch of deep water separating the eastern from the western Atlantic, and (4) the freshwater plume of the Orinoco and the Amazon rivers between the Caribbean and the coast of Brazil. These barriers have previously been shown to be important in at least a subset of the shallow water marine organisms in which phylogeography has been studied. In contrast, the Eastern Pacific Barrier, 5000 km of deep water between the central and the eastern Pacific that has caused the deepest splits in other genera of sea urchins, is remarkably unimportant as a cause of genetic subdivision in Tripneustes. There is also no discernible subdivision between the Pacific and Indian Ocean populations of this genus. The most common COI haplotype is found in the eastern, central, and western Pacific as well as the Indian Ocean. Morphology, COI, and bindin data agree that T. depressus from the eastern Pacific and T. gratilla from the western Pacific are, in fact, the same species. The distribution of haplotype differences in the Indo-Pacific exhibits characteristics expected from a sea urchin genus with ephemeral local populations, but with high fecundity, dispersal, and growth: there is little phylogenetic structure, and mismatch distributions conform to models of recent population expansion on a nearly global scale. Yet, comparisons between local populations produce large and significant F ST values, indicating nonrandom haplotype distribution. This apparent local differentiation is only weakly reflected in regional divergence, and there is no evidence of isolation by distance in correlations between F ST values and either geographical or current distance. Thus, Tripneustes in the Indo-Pacific (but not in the Atlantic) seems to be one large metapopulation spanning two oceans and containing chaotic, nonequilibrium local variation, produced by the haphazard arrival of larvae or by unpredictable local extinction. To understand how allopatric speciation proceeds, we must deduce the nature, efficacy, and timing of barriers to gene flow between populations. For marine organisms with planktonic larvae, identification of such barriers is difficult, because these propagules disperse to an unknown extent in unpredictable directions. In broad outline, obstacles to di...

Crucibles of creativity: the geographic origins of tropical molluscan innovations

“…This phylogenetic separation, indicated by a deep split between IWP and AEP clades, is well-documented for corals (Fukami et al 2004), echinoids (Lessios 2001;Lessios et al 1999Lessios et al , 2001Lessios et al , 2003, fishes (Bowen et al 2001;Streelman et al 2002;Floeter et al 2008;Cooper et al 2009), hermit crabs (Malay and Paulay 2010), and molluscs (Meyer 2003(Meyer , 2004Williams and Reid 2004;Ozawa 2004, 2007;Duda and Kohn 2005;Latiolais et al 2006;Williams 2007;Claremont et al 2008;Frey and Vermeij 2008;Reid et al 2008Reid et al , 2010Kirkendale 2009;Malaquias and Reid 2009;Reijnen et al 2010). Paleontological evidence indicates that the split was already evident during the Late Oligocene, before the Tethys seaway linking the two realms was closed in the Early Miocene (19 Ma) and definitively ceased to exist after the Middle Miocene (Langhian, 16 Ma) (Harzhauser et al 2002(Harzhauser et al , 2007Harzhauser 2009).…”

Evolutionary animation: How do molecular phylogenies compare to Mayr's reconstruction of speciation patterns in the sea?

“…Molecular phylogenies have revealed this statement to hold true for Eucidaris (9), Diadema (13), and Echinometra (11), although in the latter two genera there are indications that larvae are occasionally able to breach the barrier, which may represent the early stages leading toward secondary sympatry. Tripneustes in the Indo-Pacific, on the other hand, shows no evidence that its gene flow is in any way impeded by the 5,000 km of deep open water between Clipperton and the Marquesas (8), and a similar situation exists for Echinothrix, an Indo-Pacific genus of sea urchins that appears to have recently colonized the eastern Pacific (23,29). It is unclear why some species are able to traverse the barrier so easily when the majority cannot, because there are no pronounced differences in the length of the competent larval stage of the genera.…”

“…The genus Tripneustes shows a pattern of dissimilar geographic distribution of genetic variation in two major oceanic regions (8).…”

Highly contrasted population genetic structures in a host–parasite pair in the Caribbean Sea

“…This pattern was previously detected within the Caribbean in other taxonomic groups (Johnston et al., 2012 ; Purcell et al., 2006; Silberman et al., 1994), as well as in other sea urchins (Lessios, Kane, & Robertson, 2003; Lessios, Kessing, & Pearse, 2001; Lessios et al., 2012; McCartney, Keller, & Lessios, 2000; Zigler & Lessios, 2004). The present study confirms this last observation, not only for mitochondrial DNA, but also for microsatellites.…”

“…This temporal pattern coincides with both the expansions calculated from mismatch and EBSP analyzes. A similar population expansion was also suggested for two Caribbean squirrelfishes (Bowen, Bass, Muss, Carlin, & Robertson, 2006), for a corallivorous mollusk (Johnston et al., 2012), for a sea urchin (Lessios et al., 2003), and for a pea crab (Ocampo et al., 2013). This expansion might be linked to an increase in habitat availability during interglacial periods.…”