Phylogeography of the Pantropical Sea Urchin Eucidaris in Relation to Land Barriers and Ocean Currents
Total Page：16
File Type：pdf, Size：1020Kb
Evolution, 53(3), 1999, pp. 806-817 PHYLOGEOGRAPHY OF THE PANTROPICAL SEA URCHIN EUCIDARIS IN RELATION TO LAND BARRIERS AND OCEAN CURRENTS H. A. LESSIOS,1,2 B. D. KESSING,1 D. R. ROBERTSON,1 AND G. PAULAY3 1SmithsonianTropical Research Institute,Box 2072, Balboa, Panama 2E-mail. lessiosh@ naos.si. edit 3MarineLaboratory, University of Guam, Mangilao, Guam 96923, USA E-mail: gpaulay@ uog9.uog. edu Abstract.-Thepantropical sea urchingenus Eucidaris contains four currently recognized species, all ofthem allopatric: E. metulariain theIndo-West Pacific, E. thouarsiin theeastern Pacific, E. tribuloidesin boththe westernand eastern Atlantic, and E. clavata at the central Atlantic islands of Ascension and St. Helena. We sequenced a 640-bp region of the cytochromeoxidase I (COI) gene of mitochondrialDNA to determinewhether this division of the genusinto species was confirmedby molecularmarkers, to ascertaintheir phylogenetic relations, and to reconstructthe history of possible dispersaland vicarianceevents that led to present-daypatterns of species distribution.We foundthat E. metulariasplit first from the rest of theextant species of thegenus. If COI divergenceis calibratedby theemergence of the Isthmusof Panama, the estimateddate of the separationof the Indo-WestPacific species is 4.7-6.4 million yearsago. This date suggeststhat the last available routeof geneticcontact between the Indo-Pacificand therest of the tropicswas fromwest to east throughthe EasternPacific Barrier, rather than through the Tethyan Sea or around the southerntip of Africa.The secondcladogenic event was the separationof easternPacific and Atlanticpopulations by the Isthmusof Panama.Eucidaris at the outereastern Pacific islands (Galapagos, Isla del Coco, ClippertonAtoll) belong to a separateclade, so distinctfrom mainland E. thouarsias to suggestthat this is a differentspecies, for whichthe name E. galapagensisis revivedfrom the older taxonomicliterature. Complete lack of sharedalleles in threeallozyme loci betweenisland and mainlandpopulations support their separate specific status. Eucidaris gala- pagensisand E. thouarsiare estimatedfrom their COI divergenceto have splitat aboutthe same timethat E. thouarsi and E. tribuloideswere being separatedby theIsthmus of Panama. Even thoughcurrents could easily conveylarvae betweenthe easternPacific islands and the Americanmainland, the two species do not appearto have invadedeach other'sranges. Conversely, the centralAtlantic E. clavata at St. Helena and Ascensionis geneticallysimilar to E. tribuloidesfrom the Americanand Africancoasts. Populationson these islands are eithergenetically connected to the coasts of the Atlanticor have been colonizedby extantmitochondrial DNA lineages of Eucidariswithin the last 200,000 years. Althoughit is hard to explain how larvae can cross the entirewidth of the Atlanticwithin their competentlifetimes, COI sequencesof Eucidaris from the west coast ofAfrica are very similar to thoseof E. tribuloides fromthe Caribbean.FST statisticsindicate that gene flowbetween E. metulariafrom the Indian Ocean and fromthe westernand centralPacific is restricted.Low geneflow is also evidentbetween populations of E. clavatafrom Ascension and St. Helena. Rates of intraspecificexchange of genes in E. thouarsi,E. galapagenisis, and E. tribuloides,on the otherhand, are high.The phylogenyof Eucidaris confirms Ernst Mayr's conclusions that major barriers to thedispersal of tropicalechinoids have been thewide stretchof deep waterbetween central and easternPacific, the cold wateroff the southwestcoast of Africa,and the Isthmusof Panama. It also suggeststhat a colonizationevent in the eastern Pacifichas led to speciationbetween mainland and island populations. Key words.-Biogeography,cytochrome oxidase, gene flow,islands, mitochondrial DNA, ocean currents,sea urchins. Received May 1, 1998. AcceptedJanuary 25, 1999. In 1954 Ernst Mayr published an article on geographic raphy can provide informationdifficult to obtain fromother speciation of tropical echinoids (Mayr 1954). In this paper characters, such as the existence of sibling species and the he plotted the ranges of species belonging to 16 sea urchin, timing of splits between populations (Palumbi 1996, 1997). sand dollar, and heart urchin genera as given in Mortensen's The present paper is an attemptto apply molecular tools to (1928-1951) monograph, and reached the conclusion that the species of the genus Eucidaris to evaluate Mayr's con- theirgeographic distributionswere consistentwith allopatric clusions. speciation. Geographical barriers seen by Mayr as causing Eucidaris belongs to the subclass Perischoechinoidea, sep- speciation were the wide stretchof deep water dividing the arated from all other extant Echinoidea at least since the eastern Pacific from the central Pacific (the Eastern Pacific Triassic (Durham 1966; Smith 1984). The fossil record of Barrier), the Isthmus of Panama, and the cold waters off Eucidaris dates back to the Upper Eocene (Fell 1966; Cutress southwest Africa. He wrote that the genus Eucidatris "illus- 1980), approximately50 million years ago (mya). The genus trates geographic speciation almost diagrammatically." is pantropical, with all of its species concentratedin shallow Mayr reached these conclusions while recognizing thathe water (< 570 m; Mortensen 1928-195 1). Its fourrecognized was dealing with morphospecies ratherthan biological spe- morphospecies have adjacent but nonoverlapping geograph- cies and that echinoid systematics were still at the stage of ical distributions.Eucidaris metularia ranges from the east alpha taxonomy. We now have the tools to investigate what coast of Africa to the central Pacific. Eucidaris thouarsi is Avise et al. (1987) have called "phylogeography," that is, found in the eastern Pacific. Eucidaris tribuloides is distrib- intra- and interspecificphylogenies, which in combination uted fromthe Atlantic coast of tropical America to the west- with distributionalinformation can help deduce patternsand ern coast of Africa. Eucidaris clavata is endemic to the central causes of divergence and speciation. Molecular phylogeog- Atlantic islands of Ascension and St. Helena. The morpho- 806 ?) 1999 The Society forthe Study of Evolution. All rightsreserved. This content downloaded on Thu, 17 Jan 2013 14:37:51 PM All use subject to JSTOR Terms and Conditions PHYLOGEOGRAPHY OF EUCIDARIS 807 logical differencesbetween the species are slight. There are DNA extractions, polymerase chain reaction (PCR) ampli- doubts in the taxonomic literatureas to whether the Gala- fication,PCR productpurification, and DNA sequencing were pagos populations of Eucidaris belong to E. thouarsi or carried out as described previously (Lessios et al. 1998). whether they constitute a separate species, E. galapagensis Primers for both PCR and sequencing were: either COI-f 5' (Mortensen 1928-195 1, vol. I, p. 399) and as to whetherE. (CCTGCAGGAGGAGGAGAYCC) or COI-p 5' (GGTCA- clavata is a separate species fromE. tribuloides(Mortensen CCCAGAAGTGTACAT) and COI-a 5' (AGTATAAGC- 1928-1951, vol. I, p. 411). Eucidaris tribuloides on the Af- GTCTGGGTAGTC). All individuals were sequenced in both rican coast has been recognized as a separate subspecies, E. directions. Phylogenies from mtDNA data were constructed tribuloides africana (Mortensen 1928-1951, vol. I, p. 406). withtest version 4.0d64 of PAUP*, writtenby David L. Swof- We used sequence data from a 640-bp fragmentof the ford and used with his permission, and with PUZZLE 4.0, cytochrome oxidase I (COI) region of mitochondrial DNA writtenby Strimmerand von Haeseler (1996). Other analyses (mtDNA) and isozymes to determinethe validity of species were performedwith SEQUENCER 4.0, an Apple Macintosh described on the basis of morphology and to ascertain their program writtenby B. D. Kressing and available fromhim. phylogenetic relations. Specifically, we were interested in Sequences have been deposited in GenBank under accession answering the following questions: (1) Is each geographic nos. AF063309-AF063399 and AF107700-AF107721. isolate a separate evolutionary lineage? (2) To what extent do the accepted morphospecies coincide withmtDNA clades? Isozymes (3) What is the order and timing of cladogenic events, and what can theytell us about the effectsof presumed geographic Because the COI sequence data indicated that Eucidaris barriers on the speciation of tropical marine organisms? from the outer eastern Pacific islands (Galapagos, Isla del Coco, and Clipperton) were a distinctlineage fromE. thouarsi MATERIALS AND METHODS from the American coast (see results), isozymes were used to determine whether genetic discontinuities in the eastern Collections Pacific extended to the nuclear genome. Twelve loci were assayed in animals fromthe Galapagos and Isla del Coco in One hundredtwelve individuals were collected formtDNA the same buffersand with the same staining recipes as those sequencing at the following locations for each species (see of Berminghamand Lessios (1993). The data were compared Fig. 1): E. metularia: Reunion, Indian Ocean (n = 4); Ishi- with data from the same loci obtained previously by these gaki-Jima,Sakishima Islands, Japan (n = 2); Sesoko, Oki- authorsfrom coastal populations at Mexico and Panama. Pre- nawa-Jima,Ryukyu Islands, Japan (n = 4); Guam, west Pa- sumptive alleles were standardized by running individuals cific (n = 5); and Hawaii (n = 15, two specimens fromLanai, fromPanama on the same gels as those fromGalapagos and one fromMaui, 12 fromOahu); E. thouarsi: Galapagos