Advertisement

Conservation Genetics

, Volume 8, Issue 4, pp 797–807 | Cite as

Riverbeds demarcate distinct conservation units of the radiated tortoise (Geochelone radiata) in southern Madagascar

  • Sébastien Rioux Paquette
  • Sandra M. Behncke
  • Susan H. O’Brien
  • Rick A. Brenneman
  • Edward E. LouisJr.
  • François-Joseph Lapointe
Original Paper

Abstract

The radiated tortoise (Geochelone radiata) is an endangered species endemic to Madagascar. It inhabits the semiarid spiny forest of the southern part of the island, an ecosystem heavily affected by habitat destruction. Furthermore, illegal harvesting greatly threatens this species. The main objective of our study was to acquire better knowledge of its genetic structure, in order to take appropriate management decisions concerning, for instance, the reintroduction of confiscated individuals. Our hypothesis was that rivers represent effective barriers to tortoise dispersal despite the fact that they are dry most of the year. We used 13 polymorphic microsatellite markers to compare samples from six populations across the range of the species. All analyses (Fisher’s exact tests, F ST values, AMOVA) indicated that the radiated tortoise exhibits moderate levels of genetic structure throughout its range. In addition, we used a multiple regression approach that revealed the importance of rivers to explain the observed structure. This analysis supported the role of the Menarandra and Manambovo Rivers as major barriers to the dispersal of most radiated tortoises, but Markov chain Monte Carlo simulations revealed that low levels of recurrent gene flow may explain why F ST values were not higher. We identified three distinct conservation units with relatively high assignments rates (87%), which should be valuable for the management of the species. This is the first study to report the genetic structure of a species sampled throughout the Malagasy spiny forest.

Keywords

Genetic structure Management units Microsatellites Radiated tortoise Madagascar 

Notes

Acknowledgements

This study was in part supported by a NSERC scholarship, a FES scholarship from Université de Montréal and a scholarship from the Agence Universitaire de la Francophonie (AUF) to S.R.P., and NSERC grant no. 0155251 to F.J.L. This research was further supported by the Ahmanson Foundation, which provided the laboratory at the Henry Doorly Zoo with three ABI automated sequencers. This project would not have been possible without the support of the Institute for Conservation of Tropical Environments, Madagascar (ICTE-MICET), the Parc Botanique et Zoologique de Tsimbazaza (PBZT), the Université de Tuléar, the Centre Écologique de Libanona (CEL) at Fort-Dauphin, the Association Nationale pour la Gestion des Aires Protégées (ANGAP) and the Ministère des Eaux et Forêts of Madagascar. Deeply appreciated additional logistical assistance was provided by the staff of WWF at Tulear and Fort-Dauphin, and by the staff of ANGAP at Bezaha-Mahafaly Special Reserve and at Andohahela National Park. Special thanks go to all local guides, cooks and drivers from southern Madagascar, to Ny Andry Ranarivelo (ANGAP), Jules Médard (PBZT), Emahalala Ellis (CEL) and Vicki Beard for their invaluable help in the field, and to Barry Ferguson for making this project possible. We also wish to thank P. Palsboll and two anonymous reviewers for critical comments that considerably improved the manuscript, and members of the Laboratoire d’Écologie Moléculaire et Évolution (LEMEE) for their help in the lab and with the redaction.

References

  1. Behler J (2002) Madagascar Tortoise Crisis. Turtle Tortoise Newslett 5:18–19Google Scholar
  2. Banks MA, Eichert W, Olsen JB (2003) Which genetic loci have greater population assignment power? Bioinformatics 19:1436–1438PubMedCrossRefGoogle Scholar
  3. Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:595–606Google Scholar
  4. Battistini R (1964) Étude Géomorphologique de l’Extrême-Sud de Madagascar. Éditions Cujas, Paris, FranceGoogle Scholar
  5. Battistini R (1971) Conditions de gisements des sites littoraux de sub-fossiles et causes de la disparition des grands animaux dans le Sud-Ouest et l’Extrême-Sud de Madagascar. Taloha 4:7–18Google Scholar
  6. Burney DA (1993) Late Holocene changes in arid southwestern Madagascar. Quat Res 40:98–106CrossRefGoogle Scholar
  7. Burney DA (1997) Theories and facts regarding Holocene environmental change before and after human colonization. In: Goodman SM, Patterson BD (eds) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, DC, pp 75–89Google Scholar
  8. Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol Ecol 12:2907–2918PubMedCrossRefGoogle Scholar
  9. Ciofi C, Milinkovitch MC, Gibbs JP, Caccone A, Powell JR (2002) Microsatellite analysis of genetic divergence among populations of giant Galapagos tortoises. Mol Ecol 11:2265–2283PubMedCrossRefGoogle Scholar
  10. Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000PubMedGoogle Scholar
  11. Crandall KA, Binida-Edmonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  12. Cunningham J, Baard EHW, Harley EH, O’Ryan C (2002) Investigation of genetic diversity in fragmented geometric tortoise (Psammobates geometricus) populations. Conserv Genet 3:215–223CrossRefGoogle Scholar
  13. Du Puy DJ, Moat J (2003) Using geological substrate to identify and map primary vegetation types in Madagascar and the implication for planning biodiversity conservation. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, Illinois, pp 51–67Google Scholar
  14. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  15. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedGoogle Scholar
  16. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  17. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  18. Green DM (2005) Designatable units for status assessment of endangered species. Conserv Biol 19:1813–1820CrossRefGoogle Scholar
  19. Hey J (2005) On the number of New World Founders: A population genetic portrait of the peopling of the Americas. PLoS Biol 3:e193PubMedCrossRefGoogle Scholar
  20. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with application to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
  21. Hey J, Won YJ, Sivasundar A, Nielsen R, Markert JA (2004) Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol 13:909–919PubMedCrossRefGoogle Scholar
  22. Hoerner JM (1981) Tuléar et le sud-ouest de Madagascar: Approche démographique. Madagascar Rev Geogr 39:9–49Google Scholar
  23. Juvik JO (1975) The radiated tortoise of Madagascar. Oryx 13:145–148CrossRefGoogle Scholar
  24. Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv. Genet. (In press) DOI 10.1007/s10592–006–9134–9Google Scholar
  25. King TL, Julian SE (2004) Conservation of microsatellite DNA flanking sequences across 13 Emydid genera assayed with novel bog turtle (Glyptemys mulhenbergii) loci. Conserv Genet 5:719–725CrossRefGoogle Scholar
  26. Knapen D., Knaepkens G., Bervoets L, Taylor MI, Eens M, Verheyen E (2003) Conservation unis based on mitochondrial and nuclear DNA variation among European bullhead populations (Cottus gobio L., 1758) from Flanders, Belgium. Conserv Genet 4:129–140CrossRefGoogle Scholar
  27. Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior: a permutational regression approach. Evolution 48:1487–1499. Permute! program available online at http://www.bio.umontreal.ca/legendre/indexEnglish.htmlGoogle Scholar
  28. Leuteritz TEJ (2002) Distribution, Status and Reproductive Biology of the Radiated Tortoise, Geochelone radiata (Shaw, 1802) in Southwest Madagascar. PhD thesis, George Mason University, Fairfax, VirginiaGoogle Scholar
  29. Leuteritz TEJ, Lamb T, Limberaza JC (2005) Distribution, status and conservation of radiated tortoises (Geochelone radiata) in Madagascar. Biol Conserv 124:451–461CrossRefGoogle Scholar
  30. Leuteritz TEJ, Ravolanaivo R (2005) Reproductive biology and egg production of the radiated tortoise (Geochelone radiata) in southwest Madagascar. African Zool 40:233–242Google Scholar
  31. Lewis PO, Zaykin D (2001) Genetic Data Analysis (GDA): Computer program for the analysis of allelic data (version 1.1). Available online at http://hydrodictyon.eeb.uconn.edu/people/plewis/software.phpGoogle Scholar
  32. Lewis R (1995) Status of the radiated tortoise (Geochelone radiata). Unpublished report, WWF, Antananarivo, MadagascarGoogle Scholar
  33. Lingard M, Raharison N, Rabakonandrianina E, Rakotoarisoa JA, Elmqvist T (2003) The role of local taboos in conservation and management of species: the radiated tortoise in southern Madagascar. Conserv Soc 1:223–246Google Scholar
  34. Longmire JL, Gee GF, Hardekoff CL, Mark GA (1992) Establishing paternity in whooping cranes (Grus americana) by DNA analysis. The Auk 109:522–529Google Scholar
  35. Mahé J, Sourdat M (1972) Sur l’extinction des vertébrés sub-fossiles et l’aridification du climat dans le Sud-Ouest de Madagascar. Bull Soc Geol France 14:295–309Google Scholar
  36. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  37. Michalakis Y, Excoffier L (1996) A genetic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064PubMedGoogle Scholar
  38. Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  39. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228CrossRefGoogle Scholar
  40. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
  41. Nussbaum RA, Raxworthy CJ (2000) Commentary on conservation of “Sokatra”, the radiated tortoise (Geochelone radiata) of Madagascar. Amphibian Reptile Conserv 2:6–14Google Scholar
  42. O’Brien S (2002) Population Dynamics and Exploitation of the Radiated Tortoise Geochelone radiata in Madagascar. PhD thesis, University of Cambridge, Cambridge, UKGoogle Scholar
  43. O’Brien S, Emahalala ER, Beard V, Rakotondrainy RM, Reid A, Raharisoa V, Coulson T (2003) Decline of the Madagascar radiated tortoise (Geochelone radiata) due to overexploitation. Oryx 37:338–343CrossRefGoogle Scholar
  44. Olson D, Dinerstein E (1998) The Global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv Biol 12:502–515CrossRefGoogle Scholar
  45. Pabijan M., Babik W, Rafinski J. (2005) Conservation units in north-eastern populations of the Alpine newt (Triturus alpestris). Conserv Genet 6:307–312CrossRefGoogle Scholar
  46. Palsboll PJ, Bérubé M, Aguilar A, Notarbartolo-Di-Sciara G, Nielsen R (2004) Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. Evolution 58:670–675PubMedGoogle Scholar
  47. Pennock DS, Dimmick WW (1997) Critique of the evolutionarily significant units as a definition for ‘distinct population segments’ under the U.S. Endangered Species Act Conserv Biol 11:611–619Google Scholar
  48. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudoin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  50. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201PubMedCrossRefGoogle Scholar
  51. Raxworthy CJ (2003) Introduction to the reptiles. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, Illinois, pp 934–949Google Scholar
  52. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenism. J Hered 86:248–249. Current version available online at http://www.wbiomed.curtin.edu.au/genepopGoogle Scholar
  53. Rice WE (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  54. Rioux Paquette S, Shore GD, Behncke SM, Lapointe FJ, Louis Jr EE (2005) Characterization of polymorphic microsatellite markers for the endangered Malagasy radiated tortoise (Geochelone radiata). Mol Ecol Notes 5:527–530CrossRefGoogle Scholar
  55. Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  56. Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.0: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva, Switzerland. Available from http://anthropologie.unige.ch/arlequinGoogle Scholar
  57. Schwartz TS, Karl SA (2005) Population and conservation genetics of the gopher tortoise (Gopherus polyphemus). Conserv Genet 6:917–928CrossRefGoogle Scholar
  58. Seddon N, Tobias J, Yount JW, Ramanampamonjy JR, Butchart S, Randrianizahana H. (2000) Conservation issues and priorities in the Mikea Forest of south-west Madagascar. Oryx 34:287–304CrossRefGoogle Scholar
  59. Sites JW, FitzSimmons NN, da Silva Jr NJ, Cantarelli VH (1999) Conservation genetics of the Giant Amazon River Turtle (Podocnemis expansa: Pelomedusidae) – Inferences from two classes of molecular markers. Chelonian Conserv Biol 3:454–463Google Scholar
  60. Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16PubMedCrossRefGoogle Scholar
  61. Tessier N, Lapointe FJ (2003) Comparative efficiency of different sampling techniques to obtain DNA from freshwater turtles. Chelonian Conserv Biol 4:710–712Google Scholar
  62. Tessier N, Rioux Paquette S, Lapointe FJ (2005) Conservation genetics of the wood turtle (Glyptemys insculpta) in Quebec, Canada. Can J Zool 83:765–772CrossRefGoogle Scholar
  63. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  64. Vogler AP, DeSalle R (1994) Diagnosing units of conservation management. Conserv Biol 8:354–363CrossRefGoogle Scholar
  65. Waples RS (1991) Pacific salmon, Oncorhyncus spp., and the definition of ‘species’ under the Endangered Species Act. Mar Fish Rev 53:11–22Google Scholar
  66. Won YJ, Hey J (2005) Divergence population genetics of chimpanzees. Mol Biol Evol 22:297–307PubMedCrossRefGoogle Scholar
  67. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  68. Yoder AD, Olson LE, Hanley C, Heckman KL, Rasoloarison R, Russell AL, Ranivo J, Soarimalala V, Karanth KP, Raselimanana AP, Goodman SM (2005) A multidimensional approach for detecting species patterns in Malagasy vertebrates. Proc Natl Acad Sci USA 102:6584–6594Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Sébastien Rioux Paquette
    • 1
  • Sandra M. Behncke
    • 2
  • Susan H. O’Brien
    • 3
  • Rick A. Brenneman
    • 2
  • Edward E. LouisJr.
    • 2
  • François-Joseph Lapointe
    • 1
  1. 1.Département de Sciences BiologiquesUniversité de MontréalMontréalCanada
  2. 2.Center for Conservation and ResearchHenry Doorly ZooOmahaUSA
  3. 3.Macaulay InstituteAberdeenUK

Personalised recommendations