Phylogeography of the Pantropical Sea Urchin Eucidaris in Relation to Land Barriers and Ocean Currents

Abstract

Abstract.-The pantropical sea urchin genus Eucidaris contains four currently recognized 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 Ascension 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 phylogenetic relations, and to reconstruct the history of possible dispersal and vicariance events that led to present-day patterns of species distribution. We found that E. metularia split first from the rest of the extant species 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 Pacific species is 4.7-6.4 million years ago. This date suggests that the last 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. The second cladogenic event was the separation of eastern Pacific and Atlantic populations by the Isthmus of Panama. Eucidaris at the outer eastern Pacific islands (Galapagos, Isla del Coco, Clipperton Atoll) belong to a separate 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 allozyme loci between island and mainland populations support their separate specific status. Eucidaris galapagensis and E. thouarsi are estimated from their 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 and Ascension is genetically similar to E. tribuloides from the American and African coasts. Populations on these islands are either genetically connected to the coasts of the Atlantic or have been colonized by extant mitochondrial 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 within their competent lifetimes, COI sequences of Eucidaris from the west coast of Africa are very similar to those of E. tribuloides from the Caribbean. FST statistics indicate that gene flow between E. metularia from the Indian 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. galapagenisis, and E. tribuloides, on the other hand, are hi...

Molecular phylogenetics and biogeography of transisthmian and amphi-Atlantic needlefishes (Belonidae: Strongylura and Tylosurus): perspectives on New World marine speciation

“…regalis group (Banford et al, 1993). In general, however, our findings and those of others (Lessios et al, 1999(Lessios et al, , 2000Muss et al, 2001;Scheltema, 1973Scheltema, , 1995 do not fully support RosenÕs hypothesis for relationships of New World to eastern Atlantic faunas and the timing of these events. Specifically as an example, the relationship of S. timucu and S. senegalensis indicates a very recent separation of transAtlantic species and includes the possibility of dispersal playing a central role.…”

Phylogeography of the sand dollar genus Mellita: Cryptic speciation along the coasts of the Americas

“…Molecular phylogenies of regular echinoids (Lessios et al, 1999(Lessios et al, , 2001(Lessios et al, , 2003McCartney et al, 2000;Zigler and Lessios, 2004;Palumbi and Lessios, 2005) have agreed with Mayr's (1954) model of allopatric speciation. However, our data revealed that not all divergence highlighted in this study fits an allopatric model.…”

“…However, one species of Mellita, M. grantii Mortensen, 1948, proved problematic for Mayr (1954) and he chose to ignore it in his analysis, stating that Mortensen (1948) had described M. grantii based on a single specimen from the midst of the range of M. longifissa Michelin, 1858. Mayr's (1954 model of allopatric speciation in echinoids has been supported by molecular phylogenies of regular sea urchins (Lessios et al, 1999(Lessios et al, , 2001(Lessios et al, , 2003(Lessios et al, , 2012McCartney et al, 2000;Zigler and Lessios, 2004;Palumbi and Lessios, 2005), but to-date this hypothesis has not been tested with a molecular phylogeny of a sand dollar genus.…”

Molecular systematics, historical ecology, and phylogeography of Halimeda (Bryopsidales)

“…Widespread occurrence of extant species, even on remote archipelagos (e.g., Drew, 1995;Hillis-Colinvaux, 1980Taylor, 1950;Tsuda and Kamura, 1991;Tsuda and Wray, 1977) and pan-tropical patterns of fossil ones prior to the vicariant events (Elliott, 1981;Fl€ u ugel, 1988) suggest long-distance dispersal. Such dispersal in marine organisms is considered to be a function of larval endurance in the plankton, active migrating or drifting capability, (ir)-regularity of ocean current patterns, seawater temperature tolerance limits, and habitat availability (seaweeds: Prud'homme van Reine and Van den Hoek, 1988, 1990Van den Hoek, 1987, corals: Veron, 1995, fish: Bowen et al, 2001Colborn et al, 2001;Muss et al, 2001, and sea urchins: Lessios et al, 1999Lessios et al, , 2001. Although calcified thalli of Halimeda are unlikely drifters, uncalcified juvenile stages, which grow slowly for extended periods (Meinesz, 1980), could hitchhike across the ocean on drift material (Woelkerling, 1975).…”