Insight into an island radiation: the Tarentola geckos of the Cape Verde archipelago
Raquel Vasconcelos
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal
Departamento de Zoologia e Antropologia, Faculdade de Ciências da Universidade do Porto Pr. Gomes Teixeira, 4099-002 Porto, Portugal
Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain
Search for more papers by this authorCorresponding Author
Salvador Carranza
Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain
Salvador Carranza, Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain.E-mail: [email protected]Search for more papers by this authorD. James Harris
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal
Departamento de Zoologia e Antropologia, Faculdade de Ciências da Universidade do Porto Pr. Gomes Teixeira, 4099-002 Porto, Portugal
Search for more papers by this authorRaquel Vasconcelos
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal
Departamento de Zoologia e Antropologia, Faculdade de Ciências da Universidade do Porto Pr. Gomes Teixeira, 4099-002 Porto, Portugal
Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain
Search for more papers by this authorCorresponding Author
Salvador Carranza
Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain
Salvador Carranza, Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain.E-mail: [email protected]Search for more papers by this authorD. James Harris
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal
Departamento de Zoologia e Antropologia, Faculdade de Ciências da Universidade do Porto Pr. Gomes Teixeira, 4099-002 Porto, Portugal
Search for more papers by this authorAbstract
Aim To reassess the relationships between Tarentola geckos from the Cape Verde Islands by including specimens from all islands in the range. To determine the variation within forms by sequencing over 400 specimens, thereby allowing the discovery of cryptic forms and resolving some of the issues raised previously. This extensive sampling was also used to shed light on distributions and to explain genetic diversity by comparing the ages and ecological and geological features of the islands (size, elevation and habitat diversity).
Location The Cape Verde Islands: an oceanic archipelago belonging to the Macaronesian biogeographic region, located around 500 km off Senegal.
Methods A total of 405 new specimens of Tarentola geckos were collected from nine islands with very different geological histories, topography, climate and habitats. Mitochondrial cytochrome b (cyt b) gene and 12S rRNA partial sequences were obtained and analysed using phylogenetic methods and networks to determine molecular diversity, demographic features and phylogeographic patterns.
Results The phylogenetic relationships between all known forms of Cape Verdean Tarentola specimens were estimated for the first time, the relationships between new forms were assessed and previously hypothesized relationships were re-examined. Despite the large sample size, low intraspecific diversity was found using a 303-bp cyt b fragment. Star-like haplotype networks and statistical tests suggest the past occurrence of a rapid demographic and geographical expansion over most of the islands. Genetic variability is positively correlated with size, elevation and habitat diversity of the islands, but is not linearly related to the age of the islands. Biogeographical patterns have, in general, high concordance with phylogenetic breaks and with the three eco-geographical island groups. Volcanism and habitat diversity, both tightly linked with island ontogeny, as postulated by the general dynamic model of oceanic island biogeography, as well as present and historical size of the islands appear to be the main factors explaining the genetic diversity of this group.
Main conclusions The Tarentola radiation was clarified and is clearly associated with the geological and ecological features of the islands. Two factors may account for the low intraspecific variation: (1) recent volcanic activity and high ecological stress, and (2) poor habitat diversity within some islands. More studies are needed to align taxonomy with phylogenetic relationships, whereas GIS modelling may help to predict precise species distributions.
Supporting Information
Appendix S1 Types and total number of habitats for each island in the Cape Verde archipelago.
Appendix S2 Details of material and sequences used in the present study.
Appendix S3 Genetic differentiation between Tarentola populations belonging to the same network: Snn values.
Appendix S4 Variables used in the correlation analyses between genetic variability of Cape Verdean Tarentola and geographical and ecological features of the Cape Verde Islands.
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References
- Ancochea, E., Hernan, F., Cendrero, A., Cantagrel, J.M., Fuster, J.M., Ibarolla, E. & Coello, J. (1994) Constructive and destructive episodes in the building of a young oceanic island, La Palma, Canary Islands, and genesis of the Caldera de Taburiente. Journal of Volcanology and Geothermal Research, 60, 243–262.
- Angel, F. (1935) Lézards des Îles du Cap Vert, rapportés par M. le Professeur Chevalier. Description d’espèces nouvelles. Bulletin du Museum d’Histoire Naturelle, Paris, 2, 165–169.
- Angel, F. (1937) Sur la faune herpétologique de l’Archipel du Cap Vert. XII. Congrès International Zoologie, Lisbonne, 1935, 9, 1693–1700.
- Arnold, E.N., Vasconcelos, R., Harris, D.J., Mateo, J.A. & Carranza, S. (2008) 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. Zoologica Scripta, 37, 619–636.
- Barbadillo, L.J., Lacomba, J.I., Pérez-Mellado, V., Sancho, V. & López-Jurado, L.F. (1999) Anfibios y reptiles de la Península Ibérica, Baleares y Canarias. Editorial Planeta, Barcelona, Spain.
- Brehm, A., Jesus, J., Pinheiro, M. & Harris, D.J. (2001) Relationships of scincid lizards Mabuya (Reptilia: Scincidae) from the Cape Verde Islands based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 19, 311–316.
- Brown, R.P., Campos-Delgado, R. & Pestano, J. (2000) Mitochondrial DNA evolution and population history of the Tenerife skink Chalcides viridanus. Molecular Ecology, 9, 1061–1067.
- Carranza, S., Arnold, E.N., Mateo, J.A. & López-Jurado, L.F. (2000) Long-distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: Gekkonidae), revealed by mitochondrial DNA sequences. Proceedings of the Royal Society B: Biological Sciences, 267, 637–649.
- Carranza, S., Arnold, E.N., Mateo, J.A. & López-Jurado, L.F. (2001) Parallel gigantism and complex colonization patterns in the Cape Verde scincid lizards Mabuya and Macroscincus (Reptilia: Scincidae) revealed by mitochondrial DNA sequences. Proceedings of the Royal Society B: Biological Sciences, 268, 1595–1603.
- Carranza, S., Arnold, E.N., Mateo, J.A. & Geniez, P. (2002) Relationships and evolution of the North African geckos, Geckonia and Tarentola (Reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 23, 244–256.
- Carranza, S., Arnold, E.N., Geniez, P., Roca, J. & Mateo, J.A. (2008) 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. Molecular Phylogenetics and Evolution, 46, 1071–1094.
- Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.
- Cunningham, C.W. (1997) Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an iterative procedure for choosing among phylogenetic methods. Systematic Biology, 46, 464–478.
- Darwin, C. (1845) Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S. Beagle round the world, under the command of Capt. Fitz Roy. John Murray, London.
- Duarte, M.C., Rego, F., Romeiras, M.M. & Moreira, I. (2007) Plant species richness in the Cape Verde Islands – eco-geographical determinants. Biodiversity and Conservation, 17, 453–466.
- Duprat, H.I., Friis, J., Holm, P.M., Grandvuinet, T. & Sørensen, R.V. (2007) The volcanic and geochemical development of São Nicolau, Cape Verde Islands: constraints from field and 40Ar/39Ar evidence. Journal of Volcanology and Geothermal Research, 162, 1–19.
- ESRI (2004) ArcMap 9.0. Environmental Systems Research Institute, Inc., Redlands, CA.
- Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.
- Farris, J.S., Kallersjo, M., Kluge, A.G. & Bult, C. (1994) Testing significance of incongruence. Cladistics, 10, 315–319.
- Fattorini, S. (2009) On the general dynamic model of oceanic island biogeography. Journal of Biogeography, 36, 1100–1110.
- Felsenstein, J. (1985) Confidence-limits on phylogenies – an approach using the bootstrap. Evolution, 39, 783–791.
- Frankham, R. (1997) Do island populations have less genetic variation than the mainlaind populations? Heredity, 78, 281–307.
- Fraser, D.J. & Bernatchez, L. (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology, 10, 2741–2752.
- Fu, Y.X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.
- Gómez, J.M. (2006) Salamanquesas canarias (Tarentola delalandii) en Cantabria. Boletín de la Asociación Herpetológica Española, 17, 80–81.
- Gübitz, T., Thorpe, R.S. & Malhotra, A. (2000) Phylogeography and natural selection in the Tenerife gecko Tarentola delalandii: testing historical and adaptive hypotheses. Molecular Ecology, 9, 1213–1221.
- Gübitz, T., Thorpe, R.S. & Malhotra, A. (2005) The dynamics of genetic and morphological variation on volcanic islands. Proceedings of the Royal Society B: Biological Sciences, 272, 751–757.
- Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
- Harpending, H.C., Sherry, S.T., Rogers, A.R. & Stoneking, M. (1993) Genetic structure of ancient human populations. Current Anthropology, 34, 483–496.
- Harris, D.J., Arnold, E.N. & Thomas, R.H. (1998) Relationships of the lacertid lizards (Reptilia: Lacertidae) estimated from mitochondrial DNA sequences and morphology. Proceedings of the Royal Society B: Biological Sciences, 265, 1939–1948.
- Harris, D.J., Batista, V., Lymberakis, P. & Carretero, M.A. (2004) Complex estimates of evolutionary relationships in Tarentola mauritanica (Reptilia: Gekkonidae) derived from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 30, 855–859.
- Hart, M.W. & Sunday, J. (2007) Things fall apart: biological species form unconnected parsimony networks. Biological Letters, 3, 509–512.
- Hobohm, C. (2000) Plant species diversity and endemism on islands and archipelagos, with special reference to the Macronesian Islands. Flora, 195, 9–24.
- Hudson, R.R. (2000) A new statistic for detecting genetic differentiation. Genetics, 155, 2011–2014.
- Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
- Jarvis, A., Reuter, H.I., Nelson, A. & Guevara, E. (2006) Hole-filled seamless SRTM data, Version 3 . International Centre for Tropical Agriculture (CIAT), Colombia. Available at: http://srtm.csi.cgiar.org/ (accessed September 2008).
- Jesus, J., Brehm, A. & Harris, D.J. (2002) Relationships of Tarentola (Reptilia: Gekkonidae) from the Cape Verde Islands estimated from DNA sequence data. Amphibia-Reptilia, 22, 235–242.
- Jesus, J., Freitas, A.I., Lemos, A., Gonçalves, R. & Brehm, A. (2008) First record of Tarentola mauritanica (Linnaeus, 1758) on Porto Santo Island. Herpetozoa, 20, 175–177.
- Joger, U. (1984) Taxonomische revision der Gattung Tarentola (Reptilia, Gekkonidae). Bonner Zoologische Beiträge, 35, 129–174.
- Joger, U. (1993) On two collections of reptiles and amphibians from the Cape Verde Islands, with descriptions of three new taxa. Courier Forschungsinstitut Senckenberg, 159, 437–444.
- Knudsen, M.F., Abrahamsen, N. & Riisager, P. (2003) Paleomagnetic evidence from Cape Verde Islands basalts for fully reversed excursions in the Brunhes Chron. Earth and Planetary Science Letters, 206, 199–214.
- Kocher, T.D., Thomas, R.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences USA, 86, 6196–6200.
- Lalueza-Fox, C., Castresana, J., Samprieto, L., Marquès-Bonet, T., Alcover, J.A. & Bertranpetit, J. (2005) Molecular dating of caprines using ancient DNA sequences of Myotragus balearicus, an extinct endemic Balearic mammal. BMC Evolutionary Biology, 5, 70.
- Langley, C.H. & Fitch, W.M. (1974) An examination of the constancy of the rate of molecular evolution. Journal of Molecular Evolution, 3, 161–177.
- Langworthy, M. & Finan, T.J. (1997) Waiting for rain – agriculture and ecological imbalance in Cape Verde. Lynne Rienner Publishers, Boulder, CO.
- Maca-Meyer, N., Carranza, S., Rando, J.C., Arnold, E.N. & Cabrera, V.M. (2003) Status and relationships of the extinct giant Canary Island lizard Gallotia goliath (Reptilia: Lacertidae), assessed using ancient mtDNA from its mummified remains. Biological Journal of the Linnean Society, 80, 659–670.
- MacArthur, R.H. & Wilson, E.O. (1963) An equilibrium theory of insular zoogeography. Evolution, 17, 373–387.
-
MacArthur, R.H. &
Wilson, E.O. (1967) The theory of island biogeography. Princeton University Press, Princeton, NJ.
10.1111/j.1463-6409.2007.00280.x Google Scholar
- Maddison, W.P. & Maddison, D.R. (1992) MacClade, version 3: analysis of phylogeny and character evolution. Sinauer, Sunderland, MA.
- Mason-Gamer, R.J. & Kellogg, E.A. (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology, 45, 524–545.
- Mertens, R. (1955) Die Eidechsen der Kapverden. Commentationes Biologicae, 15, 1–17.
- Michkevich, M.F. & Farris, J.S. (1981) The implications of congruence in Menidia. Systematic Zoology, 30, 351–370.
- Mitchell, J.G., LeBas, M.J., Zielonka, J. & Furnes, H. (1983) On dating the magmatism of Maio, Cape Verde Islands. Earth and Planetary Science Letters, 64, 66–76.
- Mitchell-Thomé, R.C. (1976) Geology of the middle Atlantic islands. Science Publishers, Stuttgart.
- Morris, R.O. (1989) Navigational chart number 366 ‘Arquipélago de Cabo Verde’. Hydrographic Society, Taunton, UK.
- Nogales, M., López, M., Jiménez-Asensio, J., Larruga, J.M., Hernández, M. & González, P. (1998) Evolution and biogeography of the genus Tarentola (Sauria: Gekkonidae) in the Canary Islands, inferred from mitochondrial DNA sequences. Journal of Evolutionary Biology, 11, 481–494.
- Palumbi, S.R. (1996) Nucleic acids, II: the polymerase chain reaction. Molecular systematics (ed. by D.M. Hillis, C. Moritz and B.K. Mable), pp. 205–247. Sinauer Associates, Sunderland, MA.
- Pestano, J. & Brown, R.P. (1999) Geographical structuring of mtDNA in Chalcides sexlineatus within the island of Gran Canaria. Proceedings of the Royal Society B: Biological Sciences, 266, 815–823.
- Plesner, S., Holm, P.M. & Wilson, J.R. (2002) 40Ar–39Ar geochronology of Santo Antão, Cape Verde Islands. Journal of Volcanology and Geothermal Research, 120, 103–121.
- Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
- Posada, D. & Crandall, K.A. (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proceedings of the National Academy of Sciences USA, 98, 13757–13762.
- Rambaut, A. & Grassly, N.C. (1997) Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Computer Applications in the Biosciences, 13, 235–238.
- Rogers, A.R. (1995) Genetic evidence for a Pleistocene population expansion. Evolution, 494, 608–615.
- Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.
-
Rosenzweig, M.L. (1995) Species diversity in space and time. Cambridge University Press, Cambridge.
10.1111/j.2006.0906-7590.04272.x Google Scholar
- Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497.
- Sanderson, M.J. (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101–109.
- Sanderson, M.J. & Doyle, J.A. (2001) Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. American Journal of Botany, 88, 1499–1516.
- Schleich, H.H. (1987) Herpetofauna Caboverdiana. Spixiana, 12, 1–75.
- Schlüter, T. (2006) Geological atlas of Africa with notes on stratigraphy, tectonics, economic geology, geohazards and geosites of each country. Springer, Berlin.
- Schneider, S. & Excoffier, L. (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics, 152, 1079–1089.
- Schwartz, M.K., Luikart, G. & Waples, R.S. (2006) Genetic monitoring as a promising tool for conservation and management. Trends in Ecology and Evolution, 22, 25–33.
- Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16, 1114–1116.
- Slatkin, M. & Hudson, R.R. (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555–562.
- Stillman, C.J., Furnes, H., LeBas, M.J., Robertson, A.H.F. & Zielonka, J. (1982) The geological history of Maio, Cape Verde Islands. Journal of the Geological Society of London, 139, 347–361.
- Swofford, D.L. (1998) PAUP*: phylogenetic analysis using parsimony (*and other methods), v4.0. Sinauer Associates, Sunderland, MA.
- Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.
- Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmourgin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882.
- Thorpe, R.S. & Malhotra, A. (1996) Molecular and morphological evolution within small islands. Philosphical Transactions of the Royal Society B: Biological Sciences, 351, 815–822.
- Thorpe, R.S., Black, H. & Malhotra, A. (1996) Matrix correspondence tests on the DNA phylogeny of the Tenerife lacertid elucidate both historical causes and morphological adaptation. Systematic Biology, 45, 335–343.
- Torres, P.C., Silva, L.C., Serralheiro, A., Tassinari, C. & Munhá, J. (2002) Enquadramento geocronológico pelo método K/Ar das principais sequências vulcano-estratigráficas da ilha do Sal — Cabo Verde. Garcia de Orta, Série Geológica, 18, 9–13.
- Whittaker, R.J. (1998) Island biogeography: ecology, evolution, and conservation. Oxford University Press, Oxford.
- Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2008) A general dynamic theory of oceanic island biogeography. Journal of Biogeography, 35, 977–994.