Phylogeography and diversification history of the day-gecko genus Phelsuma in the Seychelles islands

BMC Evolutionary Biology

D James Harris²  David Posada¹  Sara Rocha¹ 

[1] Departamento de Bioquímica, Genética e Inmunología, Facultad de Biología, Universidad de Vigo, Vigo 36310, Spain;Departamento de Biologia, Faculdade de Ciências, Rua do Campo Alegre, Porto FC4 4169-007, Portugal

关键词: Biogeography;    Character displacement;    Morphological evolution;    Diversification;    Species-trees;    Phylogeography;    Seychelles;    Phelsuma;   

Others  :  1130394
DOI  :  10.1186/1471-2148-13-3

 received in 2012-08-31, accepted in 2012-12-17,  发布年份 2013

【 摘 要 】

Background

Lying in a shallow continental shelf cyclically affected by oscillating sea levels since the Miocene, the Seychelles islands are particularly interesting for evolutionary studies. Recent molecular studies are generating an emerging picture of the origin of its biota, yet very little is known regarding their phylogeographic structure or on the factors promoting diversification within the archipelago. Here we aimed to obtain a detailed depiction of the genetic structure and evolution of one of the most widespread vertebrate groups in the archipelago: the day-geckos of the genus Phelsuma. In parallel, we aimed to infer divergence times between species and subspecies, testing a long-standing hypothesis that argues for different time since sympatry between species as the cause of their different morphological differentiation across the archipelago.

Results

Molecular data corroborated the existence of two main lineages, corresponding to the two currently recognized species. Divergences between species likely date back to the Mio-Pliocene, while more recent, Pleistocenic, divergences are suggested within each species. Populations from outer islands share mtDNA haplotypes with inner island populations, suggesting very recent dispersals (or introductions). We found no evidence of current gene flow between species, but results pointed to the possibility of gene flow between (now allopatric) subspecies. Time estimates suggest a synchronous divergence within each species (between island groups).

Conclusions

The geographic patterns of genetic variation agree with previous taxonomic subdivisions within each species and the origin of outer islands populations is clearly tracked. The similar intraspecific divergence time estimates obtained suggest that the differential body-size differentiation between species within each group of islands may be driven by factors other than character displacement proportional to time since sympatry, as previously suggested. These factors could include different habitats/resources available within each island group, niche differentiation and/or character displacement. We also bring again into consideration the hypothesis of body size being influenced by the distribution of native vegetation and social systems within this group, although it remains to be tested. Our results highlight not only the necessity of clarifying the role of ecology and interspecific interactions in this group’s morphological diversification and community assemblage, but also the importance of co-evolutionary mechanisms and their importance for appropriate conservation of island biodiversity. Further, we provide a detailed description of the phylogeographic structure of these taxa across these islands, which still remain poorly characterized in this respect.

【 授权许可】

   
2013 Rocha et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Mittermeier RA, Robles Gil P, Hoffman J, Pilgrim J, Brooks T, Mittermeier CG, Lamoreaux J, da Fonseca GAB: Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. Chicago: University of Chicago Press; 2005.
• [2]Cheke AS, Hume JP: Lost Land of the Dodo. An Ecological History of Mauritius, Réunion & Rodrigues. London: Yale University Press; 2008.
• [3]Gerlach J: Terrestrial and freshwater vertebrates of the Seychelles islands. Leiden: Backhuys Publishers; 2007.
• [4]Hawlitschek O, Brückmann B, Berger J, Green K, Glaw F: Integrating field surveys and remote sensing data to study distribution, habitat use and conservation status of the herpetofauna of the Comoro Islands. Zookeys 2011, 144:21-78.
• [5]Yoder AD, Nowak MD: Has vicariance or dispersal been the predominant biogeographic force in madagascar? only time will tell. Annu Rev Ecol Evol Syst 2006, 37:405-431.
• [6]Warren BH, Strasberg D, Bruggemann JH, Prys-jones RP: Cladistics Why does the biota of the madagascar region have such a strong asiatic flavour? Cladistics 2010, 26:526-538.
• [7]Agnarsson I, Kuntner M: The generation of a biodiversity hotspot: biogeography and phylogeography of the western indian ocean islands. In Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems. Edited by Anamthawat-Jónsson K. Rijeka: In Tech Publishers; 2012:33-82. ISBN 978-953-51-0217-5
• [8]Radtkey RR: Adaptive radiation of Day-geckos (Phelsuma) in the seychelles archipelago: a phylogenetic analysis. Evolution 1996, 50:604-623.
• [9]Gerlach J: Snails of the genus Pachnodus (Mollusca; Gastropoda; Enidae): their origins and evolution. J Biogeogr 1999, 26:251-255.
• [10]Silva A, Harris DJ, Rocamora G, Dufrenne A, Gerlach J, Rocha S: Assessment of mtDNA genetic diversity within the terrapins Pelusios subniger and Pelusios castanoides across the Seychelles islands. Amphibia-Reptilia 2010, 31:583-588.
• [11]Fleischer-Dogley F, Kettle CJ, Edwards PJ, Ghazoul J, Määttänen K, Kaiser-Bunbury CN: Morphological and genetic differentiation in populations of the dispersal-limited coco de mer (Lodoicea maldivica): implications for management and conservation. Divers Distrib 2011, 17:235-243.
• [12]Daniels SR: Reconstructing the colonisation and diversification history of the endemic freshwater crab (Seychellum alluaudi) in the granitic and volcanic Seychelles Archipelago. Mol Phylogenet Evol 2011, 61:534-542.
• [13]Rocha S, Harris DJ, Posada D: Cryptic diversity within the endemic prehensile-tailed gecko Urocotyledon inexpectata across the Seychelles Islands: patterns of phylogeographical structure and isolation at the multilocus level. Biol J Linn Soc 2011, 104:177-191.
• [14]Braithwaite CJR: Scientific studies in the Seychelles. In Biogeography of the Seychelles Islands. Edited by Stoddart DR. The Hague: Dr W Junk; 1984:1-16.
• [15]Plummer PS: Planet Aldabra. In Aldabra world heritage site. Edited by Amin M, Willetts D, Skerett A. Nairobi: Camerapix Publishers International; 1995:49-70.
• [16]Colonna MJ, Casanova J, Dullo WC, Camoin G: Sea level changes and ∂18O record for the past 34,000 yr from Mayotte reef, Indian Ocean. Quaternary Res 1996, 46:335-339.
• [17]Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA: Sea-level fluctuations during the last glacial cycle. Nature 2003, 423:19-24.
• [18]Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, Sugarman PJ, Cramer BS, Christie-blick N, Pekar SF: The phanerozoic record of global Sea-level change. Science 2005, 310:1293-1298.
• [19]Inger RF, Stuart BL, Iskandar DT: Systematics of a widespread Southeast Asian frog, Rana chalconota (Amphibia: Anura: Ranidae). Zool J Linn Soc-London 2009, 155:123-147.
• [20]Siler CD, Oaks JR, Esselstyn JA, Diesmos AC, Brown RM: Phylogeny and biogeography of Philippine bent-toed geckos (Gekkonidae: Cyrtodactylus) contradict a prevailing model of Pleistocene diversification. Mol Phylogenet Evol 2010, 55:699-710.
• [21]Scott H: General conclusions regarding the insect fauna of the Seychelles and adjacent islands. Trans Linn Soc Lond 2nd series (Zoology) 1933, 19:307-391.
• [22]Cheke AS: Lizards of the Seychelles. In Biogeography and ecology of the Seychelles Islands. Edited by Stoddart DR. The Hague: Dr. W. Junk; 1984:245-258.
• [23]Gerlach J, van Bruggen AC: Streptaxidae (Mollusca: Gastropoda: Pulmonata) of the Seychelles Islands, Western Indian Ocean. Zool Verh Leiden 1999, 328:1-60.
• [24]Nussbaum RA, Wu SH: Distribution, variation, and systematics of the Seychelles treefrog, Tachycnemis seychellensis (Amphibia: Anura: Hyperoliidae). J Zool 1995, 236:383-406.
• [25]Gardner AS: The systematics of the Phelsuma madagascariensis species group of day geckos (Reptilia: Gekkonidae) in the Seychelles. Zool J Linn Soc-London 1987, 91:93-105.
• [26]Nussbaum RA: The amphibians of the Seychelles. In Biogeography and ecology of the Seychelles Islands. Edited by Stoddart DR. The Hague: Dr. W. Junk; 1984:378-415.
• [27]Van Der Meijden A, Boistel R, Gerlach J, Ohler A, Vences M, Meyer A: Molecular phylogenetic evidence for paraphyly of the genus Sooglossus, with the description of a new genus of Seychellean frogs. Biol J Linn Soc 2007, 91:347-359.
• [28]Rocha S, Rösler H, Gehring P, Glaw F, Posada D, Harris DJ, Vences M: Phylogenetic systematics of day geckos, genus Phelsuma, based on molecular and morphological data (Squamata: Gekkonidae). Zootaxa 2010, 28:1-28.
• [29]Harmon LJ, Melville J, Larson A, Losos JB: The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Syst Biol 2008, 57:562-573.
• [30]Rocha S, Vences M, Glaw F, Posada D, Harris DJ: Multigene phylogeny of Malagasy day geckos of the genus Phelsuma. Mol Phylogenet Evol 2009, 52:530-537.
• [31]Cheke AS: Phelsuma GRAY 1825 in the Seychelles and neighbouring islands: a re-appraisal of their taxonomy and description of two new forms (Reptilia: Sauria: Gekkonidae). Senckenberg biol 1982, 62:181-198.
• [32]Gardner AS: The evolutionary ecology and population systematics of day-geckos genus Phelsuma in the Seychelles. Aberdeen: University of Aberdeen; 1984. [PhD thesis]
• [33]Gardner AS: Morphological evolution in the day gecko Phelsuma sundbergi in the Seychelles: a multivariate study. Biol J Linn Soc 1986, 29:223-244.
• [34]Borner AR, Minuth W: On the taxonomy of the Indian Ocean lizards of the Phelsuma madagascariensis species group (Reptilia: Geckonidae). J Bomb Nat Hist Soc 1985, 81:243-281.
• [35]Mertens R: Die nichmadagassischen arten and unterarten der geckonengattung Phelsuma. Senckenberg biol 1966, 47:85-110.
• [36]Meiri S: Size evolution in island lizards. Global Ecol Biogeogr 2007, 16:702-708.
• [37]Dayan T, Simberloff D: Ecological and community-wide character displacement: the next generation. Ecol Lett 2005, 8:875-894.
• [38]Martin PR, Montgomerie R, Lougheed SC: Rapid sympatry explains greater color pattern divergence in high latitude birds. Evolution 2010, 64:336-347.
• [39]Melo M, Warren BH, Jones PJ: Rapid parallel evolution of aberrant traits in the diversification of the Gulf of Guinea white-eyes (Aves, Zosteropidae). Mol Ecol 2011, 20:4953-4967.
• [40]Schluter D: The ecology of adaptive radiation. New York: Oxford University Press; 2000.
• [41]Ackerly DD, Schwilk DW, Webb CO: Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 2006, 87:S50-S61.
• [42]Losos JB: Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat 2010, 175:623-639.
• [43]Noble T, Bunbury N, Kaiser-Bunbury CN, Bell DJ: Ecology and co-existence of two endemic day gecko (Phelsuma) species in Seychelles native palm forest. J Zool 2011, 283:73-80.
• [44]Harmon JL, Harmon LL, Jones CG: Competition and community structure in diurnal arboreal geckos (genus Phelsuma) in the Indian Ocean. Oikos 2007, 116:1863-1878.
• [45]Carranza S, Arnold EN: A review of the geckos of the genus Hemidactylus (Squamata: Gekkonidae) from Oman based on morphology, mitochondrial and nuclear data, with descriptions of eight new species. Zootaxa 2012, 3378:1-95.
• [46]Strasburg JL, Rieseberg LH: How robust are “isolation with migration” analyses to violations of the im model? A simulation study. Mol Biol Evol 2010, 27:297-310.
• [47]Edwards SV, Beerli P: Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Gene 2000, 54:1839-1854.
• [48]Hickerson MJ, Dolman G, Moritz C: Comparative phylogeographic summary statistics for testing simultaneous vicariance. Mol Ecol 2006, 15:209-223.
• [49]Hurt C, Anker A, Knowlton N: A multilocus test of simoultaneous divergence across the isthmus of Panama using snapping shrimp in the genus Alpheus. Evolution 2009, 63:514-530.
• [50]Knowles LL: Statistical phylogeography. Annu Rev Ecol Evol Syst 2009, 40:593-612.
• [51]Wakeley J, Hey J: Estimating ancestral population parameters. Genetics 1997, 145:847-855.
• [52]Gerlach J: Population and conservation status of the reptiles of the Seychelles islands. Phelsuma 2008, 16:31-48.
• [53]Kocher TD, Thomas WK, Meyer A, Edwards SV, Paäbo S, Villablanca FX, Wilson AC: Dynamics of mitochondrial DNA evolution in animals- amplification and sequencing with conserved primers. P Natl Acad Sci USA 1989, 86:6196-6200.
• [54]Sambrook JE, Fritsh EF, Maniatis T: Molecular cloning: a laboratory manual. 2nd edition. New York: Cold Spring Harbour Press; 1989.
• [55]Austin JJ, Arnold EN, Jones CG: Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene islands. Mol Phylogenet Evol 2004, 31:109-122.
• [56]Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G: The simple Fool’s guide to PCR, version 2.0. Hawaii: Privately published; 1991.
• [57]Gamble T, Bauer AM, Greenbaum E, Jackman TR: Evidence for Gondwanan vicariance in an ancient clade of gecko lizards. J Biogeogr 2008, 35:88-104.
• [58]Pinho C, Rocha S, Carvalho BM, Lopes S, Mourão S, Vallinoto M, Brunes TO, Haddad CFB, Gonçalves H, Sequeira F, Ferrand N: New primers for the amplification and sequencing of nuclear loci in a taxonomically wide set of reptiles and amphibians. Conserv Genet Resour 2010, 2:181-185.
• [59]Hall TA: BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 1999, 41:95-98.
• [60]Flot J-F, Tillier J, Samadi S, Tillier S: Phase determination from direct sequencing of length-variable DNA regions. Mol Ecol Notes 2006, 6:627-630.
• [61]Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-989.
• [62]Watterson GA: On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975, 7:256-276.
• [63]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
• [64]Fu YX: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
• [65]Ramos-Onsins SE, Rozas J: Statistical properties of new neutrality tests against population growth. Mol Biol Evol 2002, 19:2092-2100.
• [66]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [67]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [68]Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D: ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res 2010, 38:W14-W18.
• [69]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [70]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [71]Sugiura N: Further analysis of the data by akaike’ s information criterion and the finite corrections. Commun Stat A - Theor 1978, 7:13-26.
• [72]Posada D, Buckley TR: Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol 2004, 53:793-808.
• [73]Nylander JA, Wilgenbusch JC, Warren DL, Swofford DL: AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 2008, 24:581-583.
• [74]Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9:299-306.
• [75]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
• [76]Polzin T, Daneshmand SV: On steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 2003, 31:12-20.
• [77]NETWORK v4.510. Available from http://fluxus-engineering.com webcite
• [78]Hey J, Nielsen R: Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. P Natl Acad Sci USA 2007, 104:2785-2790.
• [79]Hey J: Isolation with migration models for more than two populations. Mol Biol Evol 2010, 27:905-920.
• [80]Hasegawa M, Kishino H, Yano T: Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985, 22:160-174.
• [81]Kimura M: The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 1969, 61:893-903.
• [82]Nielsen R, Wakeley J: Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 2001, 158:885-896.
• [83]Bruen TC, Philippe H, Bryant D: A simple and robust statistical test for detecting the presence of recombination. Genetics 2006, 172:2665-2681.
• [84]Bruen T, Bruen T: PhiPack: PHI test and other tests of recombination. available at http://www.maths.otago.ac.nz/~dbryant/software.html webcite
• [85]Hudson RR, Kreitman M, Aguadé M: A test of neutral molecular evolution based on nucleotide data. Genetics 1987, 116:153-159.
• [86]Hey J: SITES and HKA. available at http://genfaculty.rutgers.edu/hey/software webcite
• [87]Heled J, Drummond AJ: Bayesian inference of species trees from multilocus data. Mol Biol Evol 2010, 27:570-580.
• [88]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
• [89]Edwards SV: Is a new and general theory of molecular systematics emerging? Evolution 2009, 63:1-19.
• [90]Leaché AD: Species trees for spiny lizards (genus Sceloporus): identifying points of concordance and conflict between nuclear and mitochondrial data. Mol Phylogenet Evol 2010, 54:162-171.
• [91]Paulo OS, Pinheiro J, Miraldo A, Bruford MW, Jordan WC, Nichols RA: The role of vicariance vs. dispersal in shaping genetic patterns in ocellated lizard species in the western Mediterranean. Mol Ecol 2008, 17:1535-1551.
• [92]Carranza S, Romano A, Arnold EN, Sotgiu G: Biogeography and evolution of European cave salamanders, Hydromantes (Urodela: Plethodontidae), inferred from mtDNA sequences. J Biogeogr 2008, 35:724-738.
• [93]Carranza S, Arnold EN, Geniez P, Roca J, Mateo JA: Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Mol Phylogenet Evol 2008, 46:1071-1094.
• [94]Arnold EN, Vasconcelos R, Harris DJ, Mateo JA, Carranza S: Systematics, biogeography and evolution of the endemic Hemidactylus geckos (Reptilia, Squamata, Gekkonidae) of the Cape Verde Islands: based on morphology and mitochondrial and nuclear DNA sequences. Zool Scr 2008, 37:619-636.
• [95]Chapple DG, Ritchie PA, Daugherty CH: Origin, diversification, and systematics of the New Zealand skink fauna (Reptilia: Scincidae). Mol Phylogenet Evol 2009, 52:470-487.
• [96]Cox SC, Carranza S, Brown RP: Divergence times and colonization of the Canary Islands by Gallotia lizards. Mol Phylogenet Evol 2010, 56:747-757.
• [97]Miralles A, Carranza S: Systematics and biogeography of the Neotropical genus Mabuya, with special emphasis on the Amazonian skink Mabuya nigropunctata (Reptilia, Scincidae). Mol Phylogenet Evol 2010, 54:857-869.
• [98]Rambaut A, Drummond AJ: Tracerv1.5. 2007. Available from http://beast.bio.ed.ac.uk/Trace webcite
• [99]Rambaut A: FigTreev1.3.1. 2009. Available from http://tree.bio.ed.ac.uk/software/figtree/ webcite