Phylogeography of the pantropical sea urchin Eucidaris in relation to landbarriers and ocean currents

The pantropical sea urchin genus Eucidaris contains four currently recogniz ed species, all of them allopatric: E. metularia in the Indo-West Pacific, E. thouarsi in the eastern Pacific, E. tribuloides in both the western and eastern Atlantic, and E. clavata at the central Atlantic islands of Ascensi on and St. Helena. We sequenced a 640-bp region of the cytochrome oxidase I (COI) gene of mitochondrial DNA to determine whether this division of the genus into species was confirmed by molecular markers, to ascertain their p hylogenetic relations, and to reconstruct the history of possible dispersal and vicariance events that led to present-day patterns of species distribu tion. We found that E. metularia split first from the rest of the extant sp ecies of the genus. If COI divergence is calibrated by the emergence of the Isthmus of Panama, the estimated date of the separation of the Indo-West P acific species is 4.7-6.4 million years ago. This date suggests that the la st available route of genetic contact between the Indo-Pacific and the rest of the tropics was from west to east through the Eastern Pacific Barrier, rather than through the Tethyan Sea or around the southern tip of Africa. T he second cladogenic event was the separation of eastern Pacific and Atlant ic populations by the Isthmus of Panama. Eucidaris at the outer eastern Pac ific islands (Galapagos, Isla del Coco, Clipperton Atoll) belong to a separ ate clade, so distinct from mainland E thouarsi as to suggest that this is a different species, for which the name E. galapagensis is revived from the older taxonomic literature. Complete lack of shared alleles in three alloz yme loci between island and mainland populations support their separate spe cific status. Eucidaris galapagensis and E. thouarsi are estimated from the ir COI divergence to have split at about the same time that E. thouarsi and E. tribuloides were being separated by the Isthmus of Panama. Even though currents could easily convey larvae between the eastern Pacific islands and the American mainland, the two species do not appear to have invaded each other's ranges. Conversely, the central Atlantic E. clavata at St. Helena a nd Ascension is genetically similar to E; tribuloides from the American and African coasts. Populations on these islands are either genetically connec ted to the coasts of the Atlantic or have been colonized by extant mitochon drial DNA lineages of Eucidaris within the last 200,000 years. Although it is hard to explain how larvae can cross the entire width of the Atlantic wi thin their competent lifetimes, COI sequences of Eucidaris from the west co ast of Africa are very similar to those of E. tribuloides from the Caribbea n. F-ST statistics indicate that gene flow between E. metularia from the In dian Ocean and from the western and central Pacific is restricted. Low gene flow is also evident between populations of E. clavata from Ascension and St. Helena. Rates of intraspecific exchange of genes in E. thouarsi, E. gal apagensis, and E. tribuloides, on the other hand, are high. The phylogeny o f Eucidaris confirms Ernst Mayr's conclusions that major barriers to the di spersal of tropical echinoids have been the wide stretch of deep water betw een central and eastern Pacific, the cold water off the southwest coast of Africa, and the Isthmus of Panama. It also suggests that a colonization eve nt in the eastern Pacific has led to speciation between mainland and island populations.