Abstract
The day gecko Phelsuma borbonica displays marked differences in coloration and occupies a variety of habitats across its very small range on the volcanic oceanic island of Reunion in the southwestern Indian Ocean. Such differences might reflect geographic and ecological divergence and thus be associated with an underlying genetic differentiation. We examined the partitioning of genetic diversity in Phelsuma borbonica across Reunion at a very small spatial scale (< 10 km) using mtDNA and nuDNA sequences, along with microsatellite genotype data. This study provides an account of the evolutionary history of Phelsuma borbonica, along with a quantification of effective population sizes, which constitute important information for the conservation of this endangered species, which may represent a previously unrecognized case of incipient speciation. We found that populations of Phelsuma borbonica are genetically strongly differentiated, highlighting historically low levels of gene flow. Phylogenetic analyses suggest that Phelsuma borbonica reached its present range through two parallel southward expansions from an ancestral population located in the northern part of the island.
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig1_HTML.jpg)
Photo credits: M. Sanchez and A. Bonanno
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig2_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig3_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig4_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig5_HTML.png)
![](https://cdn.statically.io/img/media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10592-024-01622-w/MediaObjects/10592_2024_1622_Fig6_HTML.png)
Similar content being viewed by others
References
Abdul-Muneer PM (2014) Application of microsatellite markers in conservation genetics and fisheries management: recent advances in population structure analysis and conservation strategies. Genet Res Int 2014:1–11
Arida E, Ashari H, Dahruddin H et al (2021) Exploring the vertebrate fauna of the Bird’s Head Peninsula (Indonesia, West Papua) through DNA barcodes. Mol Ecol Resour 21:2369–2387
Austin JJ, Arnold EN, Jones CG (2004) Reconstructing an island radiation using ancient and recent DNA: The extinct and living day geckos (Phelsuma) of the Mascarene islands. Mol Phylogenet Evol 31:109–122
Avise JC (2007) Twenty-five key evolutionary insights from the phylogeographic revolution in population genetics. Phylogeography of Southern European Refugia. Springer, Dordrecht, pp 7–21
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bertrand G (2000) Première mention d’un reptile à plus de 2000 mètres d’altitude (Ile de La Réunion). Bulletin Phaeton 12:110
Bertrand JAM, Bourgeois YXC, Delahaie B, Duval T, García-Jiménez R, Cornuault J, Heeb P, Milá B, Pujol B, Thébaud C (2014) Extremely reduced dispersal and gene flow in an island bird. Heredity 112:190–196
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:1003537
Brüniche-Olsen A, Kellner KF, Belant JL, Dewoody JA (2021) Life-history traits and habitat availability shape genomic diversity in birds: Implications for conservation. Proc R Soc B 288:20211441
Buckland S, Horsburgh GJ, Dawson DA, Cole NC, Krupa AP, Gallagher LE, Henshaw SM, Groombridge JJ, Harris S (2013) Isolation and characterisation of Mauritius lowland day gecko Phelsuma guimbeaui microsatellite loci. Conserv Genet Resour 5:1013–1018
Buckland S, Cole NC, Groombridge JJ, Küpper C, Burke T, Dawson DA, Gallagher LE, Harris S (2014) High risks of losing genetic diversity in an endemic Mauritian gecko: implications for conservation. PLoS ONE 9:93387
Cheek RG, Forester BR, Salerno PE, Trumbo DR, Langin KM, Chen N, Sillett TS, Morrison SA, Ghalambor CK, Funk WC (2022) Habitat-linked genetic variation supports microgeographic adaptive divergence in an island-endemic bird species. Mol Ecol 31:2830–2846
Cheke AS (1975) An undescribed gecko from Agalega: Phelsuma agalegae Sp. nov. Mauritius Inst Bull 8:33–48
Choeur A, Clémencet J, Le Corre M, Sanchez M (2022) Evidence of seasonal reproduction, laying site fidelity, and oviposition synchronicity in the critically endangered endemic Manapany Day Gecko (Phelsuma inexpectata) from Reunion Island (western Indian Ocean). Salamandra 58:116–122
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Deniel C, Kieffer G, Lecointre J (1992) New 230Th-238U and 14C age determinations from Piton des Neiges volcano, Reunion—a revised chronology for the differentiated series. J Volcanol Geoth Res 51:253–267
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214
Dong F, Li SH, Chiu CC, Dong L, Yao CT, Yang XJ (2020) Strict allopatric speciation of sky island Pyrrhula erythaca species complex. Mol Phylogenet Evol 153:106941
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
Dubos N, Augros S, Deso G, Probst J-M, Notter J-C, Roesch MA (2022) Here be dragons: important spatial uncertainty driven by climate data in forecasted distribution of an endangered insular reptile. Anim Conserv 25:704–717
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Frankham R, Ballou JD, Ralls K, Eldrige MDB, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, Oxford
Funk WC, Caminer M, Ron SR (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proc R Soc B 279:1806–1814
Gabrielli M, Nabholz B, Leroy T, Milá B, Thébaud C (2020) Within-island diversification in a passerine bird. Proc R Soc B 287:20192999
Glaw F, Rösler H (2015) Taxonomic checklist of the day geckos of the genera Phelsuma Gray, 1825 and Rhoptropella Hewitt, 1937 (Squamata: Gekkonidae). Vertebrate Zoology 65:247–283
Goudet J (2005) hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16:700–706
Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449
Harmon LJ, Melville J, Larson A, Losos JB (2008) The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Syst Biol 57:562–573
Harvey MG, Seeholzer GF, Smith BT, Rabosky DL, Cuervo AM, Brumfield RT (2017) Positive association between population genetic differentiation and speciation rates in New World birds. Proc Natl Acad Sci USA 114:6328–6333
Hauser SS, Athrey G, Leberg PL (2021) Waste not, want not: Microsatellites remain an economical and informative technology for conservation genetics. Ecol Evol 11:15800–15814
Hay EM, McGee MD, Chown SL (2022) Geographic range size and speciation in honeyeaters. BMC Ecol Evol 22:1–14
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588
Hoehn M, Sarre SD, Henle K (2007) The tales of two geckos: does dispersal prevent extinction in recently fragmented populations? Mol Ecol 16:3299–3312
Hohenlohe PA, Funk WC, Rajora OP (2021) Population genomics for wildlife conservation and management. Mol Ecol 30:62–82
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Keenan K, Mcginnity P, Cross TF, Crozier WW, Prodöhl PA (2013) DiveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788
Kim J-S, Park J, Fong JJ, Zhang Y-P, Li S-R, Ota H, Min S-H, Min M-S, Park D (2020) Genetic diversity and inferred dispersal history of the Schlegel’s Japanese Gecko (Gekko japonicus) in Northeast Asia based on population genetic analyses and paleo-species distribution modelling. Mitochondrial DNA Part A 31:120–130
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kisel Y, Barraclough TG (2010) Speciation has a spatial scale that depends on levels of gene flow. Am Nat 175:316–334
Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21:629–637
Labisko J, Maddock ST, Rocha S, Gower DJ (2022) Cryptic lineages among Seychelles Herpetofauna. In: Monro AK, Mayo SJ (eds) Cryptic species: morphological stasis, circumscription, and hidden diversity. Cambridge University Press, Cambridge, pp 242–280
Lemey P, Rambaut A, Drummond AJ, Suchard MA (2009) Bayesian phylogeography finds its roots. PLoS Comput Biol 5:e1000520
Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189
Leroy T, Rousselle M, Tilak M-K, Caizergues AE, Scornavacca C, Recuerda M, Fuchs J, Illera JC, De Swardt DH, Blanco G, Thébaud C, Milá B, Nabholz B (2021) Island songbirds as windows into evolution in small populations. Curr Biol 31:1303–1310
Liddell E, Sunnucks P, Cook CN (2021) To mix or not to mix gene pools for threatened species management? Few studies use genetic data to examine the risks of both actions, but failing to do so leads disproportionately to recommendations for separate management. Biol Conserv 256:109072
Lobo A, Hansen OK, Hansen JK, Erichsen EO, Jacobsen B, Kjær ED (2018) Local adaptation through genetic differentiation in highly fragmented Tilia cordata populations. Ecol Evol 8:5968–5976
Losos JB, Schluter D (2000) Analysis of an evolutionary species-area relationship. Nature 408:847–850
McDougall I (1971) The geochronology and evolution of the young volcanic island of Réunion, Indian Ocean. Geochim Cosmochim Acta 35:261–288
Meier H (1995) Neue Nachweise von Phelsuma borbonica auf Reunion, Maskarenen, mit dem Versuch einer taxonomischen Einordnung. Salamandra 31:33–40
Meier H, Böhme W (1990) Notes on habitat selection and colouration in life of Phelsuma borbonica agalegae. British Herpetol Soc Bull 33:4–8
Mertens R (1966) Die nichtmadagassischen Arten und Unterarten der Geckonengattung Phelsuma. Senckenberg Biol 47:85–110
Milá B, Warren BH, Heeb P, Thébaud C (2010) The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus). BMC Evol Biol 10:158
Mohan AV, Orozco-terWengel P, Shanker K, Vences M (2020) The Andaman day gecko paradox: an ancient endemic without pronounced phylogeographic structure. Sci Rep 10:1–17
Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375
Murakami Y, Sugawara H, Takahashi H, Hayashi F (2015) Population genetic structure and distribution patterns of sexual and asexual gecko species in the Ogasawara Islands. Ecol Res 30:471–478
Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259
Nei M, Tajima F (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97:145–163
Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474
Nordborg M (2004) Coalescent theory. In: Balding DJ, Bishop M, Cannings C (eds) Handbook of statistical genetics, 2nd edn. Wiley, New York
Oettinger MA, Schatz DG, Gorka C, Baltimore D (1990) RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248:1517–1523
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204
Palstra FP, Fraser DJ (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2:2357–2365
Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) Simple fool’s guide to PCR. Hawaii University Press, Hawaii
Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420
Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418
Porto Pontes F (2017) Biologia da Invasão de Hemidactylus mabouia no Brasil: Análise da Estrutura Genética Populacional. Dissertation, University of Brasilia
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Probst J-M (2003) Une nouvelle population de Phelsuma borbonica sur le Cimendef. Bull Phaeton 18:112
Probst J-M, Abhaya K (2004) Première répartition et estimation de la population de lézard vert du Maïdo. Bull Phaeton 20:109
Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:1–54
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rocha S, Posada D, Carretero MA, Harris DJ (2007) Phylogenetic affinities of Comoroan and East African day geckos (genus Phelsuma): multiple natural colonisations, introductions and island radiations. Mol Phylogenet Evol 43:685–692
Rokas A, Ladoukakis E, Zouros E (2003) Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18:411–417
Sanchez M, Probst J-M (2017) Phelsuma borbonica Mertens, 1966 (Sauria : Gekkonidae) sur l’île de La Réunion. I. Répartition et habitats naturels. Bull Soc Herpétol Fr 162:17–30
Sanchez M (2007) Ecologie d'une espèce protégée, le Lézard Vert des Hauts, Phelsuma borbonica (Mertens, 1966). Dissertation, University of Reunion
Sanchez M (2021) Phelsuma borbonica. The IUCN Red List of Threatened Species 2021: e.T17429273A17430906
Sanders KL, Lee MSY (2007) Evaluating molecular clock calibrations using Bayesian analyses with soft and hard bounds. Biol Let 3:275–279
SINP 974 (2020) Référentiel de données sensibles du Système d'information sur la nature et les paysages de La Réunion (SINP 974) v.1.4.0. https://www.borbonica.re/donnees_sensibles/. Accessed 1 June 2023
Strasberg D, Rouget M, Richardson DM, Baret S, Dupont J, Cowling RM (2005) An Assessment of habitat diversity and transformation on La Réunion Island (Mascarene Islands, Indian Ocean) as a basis for identifying broad-scale conservation priorities. Biodivers Conserv 14:3015–3032
Stroud JT, Losos JB (2016) Ecological opportunity and adaptive radiation. Annu Rev Ecol Evol Syst 47:507–532
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:1–5
Sunde J, Yıldırım Y, Tibblin P, Forsman A (2020) Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for pike (Esox lucius) and a synthesis of previous studies. Front Genet 11:218
Templeton AR (2021) Population genetics and microevolutionary theory. Wiley, New York
Templeton AR, Hemmer H, Mace G, Seal US, Shields WM, Woodruff DS (1986) Local adaptation, coadaptation, and population boundaries. Zoo Biol 5:115–125
Vacher JP, Chave J, Ficetola FG et al (2020) Large-scale DNA-based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. J Biogeogr 47:1781–1791
van der Meijden A, Crottini A, Tarrant J, Turner A, Vences M (2011) Multi-locus phylogeny and evolution of reproductive modes in the pyxicephalidae, an african endemic clade of frogs. Afr J Herpetol 60:1–12
Vergeer P, Sonderen E, Ouborg NJ (2004) Introduction strategies put to the test: Local adaptation versus heterosis. Conserv Biol 18:812–821
Vidal N, Hedges SB (2004) Molecular evidence for a terrestrial origin of snakes. Proc R Soc B 271:S226–S229
Waples RS (1991) Genetic methods for estimating the effective size of cetacean populations. Report of the International Whaling Commission 13:279–300
Waters JM, Emerson BC, Arribas P, McCulloch GA (2020) Dispersal reduction: causes, genomic mechanisms, and evolutionary consequences. Trends Ecol Evol 35:512–522
Wenne R (2023) Microsatellites as molecular markers with applications in exploitation and conservation of aquatic animal populations. Genes 14:808
Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49
Whittaker RJ, Triantis KA, Ladle RJ (2008) A general dynamic theory of oceanic island biogeography. J Biogeogr 35:977–994
Wilder AP, Navarro AY, King SND, Miller WB, Thomas SM, Steiner CC, Ryder OA, Shier DM (2020) Fitness costs associated with ancestry to isolated populations of an endangered species. Conserv Genet 21:589–601
Wright NA, Steadman DW, Witt CC (2016) Predictable evolution toward flightlessness in volant island birds. Proc Natl Acad Sci USA 113:4765–4770
Xu H, Fu YX (2004) Estimating effective population size or mutation rate with microsatellites. Genetics 166:555–563
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Zheng Y, Wiens JJ (2015) Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol 94:537–547
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121
Acknowledgements
We thank Allison Gandar, who helped with permit applications, the Nature Océan Indien NGO for support and its volunteers for field assistance, and Jean-Michel Probst for his help in starting up this project and sharing his invaluable knowledge on Mascarene Phelsuma. We thank Ivan Ineich for loaning a sample from Agalega. We thank Alicia Bonanno for kindly providing pictures. Logistic support on Reunion was provided by the Marelongue field station run by the University of Reunion and the Observatoire des Sciences de l’Université de La Réunion.
Funding
This study was supported by a Mohamed bin Zayed Species Conservation Fund grant (Project #11252997) and an Agence Française de Développement grant through Reunion National Park (convention number: 2012/PNR/012).
Author information
Authors and Affiliations
Contributions
JC, CT, MS and TD designed the study; MS did the field work; JC carried out the analyses and drafted the manuscript; all authors contributed to writing the manuscript.
Corresponding author
Ethics declarations
Competing interests
Competing interests are of a financial nature, see the Funding section.
Conflict of interest
The authors have no competing interests to declare. Authorizations Research was conducted in accordance with research application permit for protected species issued by the Reunion préfecture, and authorizations for fieldwork were kindly granted by the Reunion National Park (n°DIR/I/2011–019-036).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cornuault, J., Sanchez, M., Duval, T. et al. Deep genetic divergence underlies within-island eco-morphological variation in the endangered day gecko Phelsuma borbonica: implications for conservation. Conserv Genet (2024). https://doi.org/10.1007/s10592-024-01622-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10592-024-01622-w