Abstract
Fruit bats of the genus Pteropus are important contributors to ecosystem maintenance on islands through their roles as pollinators and seed dispersers. However, island faunas are the most prone to extinction and there is a real need to assess the possible genetic implications of population reductions in terms of extinction risk. An effective method of ameliorating extinction risk in endangered species is the establishment of captive populations ex situ. The effectiveness of captive breeding programmes may be assessed by comparing the genetic variability of captive colonies to that of wild counterparts. Here, we use polymorphic microsatellite loci to assess genetic variability in wild, critically endangered Rodrigues fruit bats (Pteropus rodricensis, Dobson 1878) and we compare this variability to that in a captive colony. We document remarkable conservation of genetic variability in both the wild and captive populations, despite population declines and founder events. Our results demonstrate that the wild population has withstood the negative effects of population reductions and that captive breeding programmes can fulfil the goals of retaining genetic diversity and limiting inbreeding.
Similar content being viewed by others
References
Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265
Ashworth D (1992) The application of DNA fingerprinting to the conservation of threatened species. Unpublished PhD thesis, University of Northampton, UK
Ballou JD, Cooper KA (1992) Genetic management strategies for endangered captive populations: the role of genetic and reproductive technology. Symp Zool Soc Lond 64:183–206
Ballou JD, Foose TJ (1996) Demographic and genetic management of captive populations. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S (eds) Wild mammals in captivity: principles and techniques. University of Chigago Press, Chigago, USA
Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (2000) GENETIX, 4.0, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome Populations Interactions, CNRS UPR 9060, Université de Montpellier II, Montpellier, France
Berthier P, Beaumont MA, Cornuet JM, Luikart G (2002) Likelihood-based estimates of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160:741–751
Black WC, Krafsur ES (1985) A FORTRAN program for the calculation and analysis of two-locus linkage disequilibrium coefficients. Theor Appl Genet 70:491–496
Burland TM, Barratt EM, Nichols RA, Racey PA (2001) Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus. Mol Ecol 10:1309–1321
Briskie JV, Mackintosh M (2004) Hatching failure increases with severity of population bottlenecks in birds. Proc Natl Acad Sci USA 101:558–561
Carroll JB, Mace GM (1988) Population management of the Rodrigues fruit bat (Pteropus rodricensis) in captivity. Int Zoo Yearb 27:70–78
Cave C (2002) Mating system of captive Rodrigues fruit bats (Pteropus rodricensis): resource defence polygyny. Unpublished thesis. National University of Ireland, Dublin
Cheke AS, Dahl JF (1981) The status of bats on western Indian Ocean islands, with special reference to Pteropus. Mammalia 45:205–238
Comeaux LB (1997) A conservation genetic study and phylogeny of three flying fox (Chiroptera: Pteropodidae) species. Unpublished Masters thesis, University of Tennessee, Knoxville, USA
Comeaux LB, McCracken GF, Whitman K (1997) Microsatellite analysis reveals high levels of genetic variation in captive and wild populations of the endangered Rodrigues Island fruit bat. Bat Res News 38:103
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Couvet D, Ronfort J (1994) Mutation load depending on variance in reproductive success and mating system. In: Loeschcke V, Tomiuk J, Jain SK (eds) Conservation genetics. Birkhaüser Verlag, Basel, Switzerland, pp 55–68
Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270
Daniel MJ (1975) First record of an Australian fruit bat (Megachiroptera: Pteropodidae) reaching New Zeland. NZ J Zool 2:227–231
Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high levels of genetic variation. Conserv Biol 4:417–422
Dudash MR, Fenster CB (2000) Inbreeding and outbreeding depression in fragmented populations. In: Young A, Clarke G (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, UK, pp 35–53
Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Marine Biol Biotechnol 5:295–298
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes, application to human mitochondrial DNA restriction data. Genetics 131:479–491
Frankham R, Manning H, Margan SH, Briscoe DA (2000) Does equalisation of family sizes reduce genetic adaptation to captivity? Anim Conserv 3:357–363
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, UK
Gaggiotti OE, Excoffier L (2000) A simple method of removing the effect of a bottleneck and unequal population sizes on pairwise genetic distances. Proc R Soc Lond B 267:81–87
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Girman DJ, Vilà C, Geffen E, Creel S, Mills MGL, McNutt JW, Ginsberg J, Kat PW, Mamiya KH, Wayne RK (2001) Patterns of population subdivision, gene flow and genetic variability in the African wild dog (Lycaon pictus). Mol Ecol 10:1703–1723
González S, Maldonado JE, Leonard JA, Vilà C, Barbanti Duarte JM, Merino M, Brum-Zorrilla N, Wayne RK (1998) Conservation genetics of the endangered Pampas deer (Ozotoceros bezoarticus). Mol Ecol 7:47–56
Goudet J (2000) FSTAT Version 2.9.1. A program to estimate and test gene diversities and fixation indices. Available from http://www.unil.ch/izea/softwares/fstat.html
Heckel G, von Helversen O (2003) Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata. Mol Ecol 12:219–227
Ingvarsson PK (2002) Lone wolf to the rescue. Nature 420:475
ISIS (2005) International Species Information System http://www.isis.org. Downloaded on 21 April, 2005
IUCN (2004) 2004 IUCN red list of threatened species http://www.redlist.org. Downloaded on 19 April, 2005
Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J Mammalogy 78:320–335
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35
Maruyama T, Fuerst PA (1985) Population bottlenecks and non-equilibrium models in population genetics II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689
McDonald-Madden E, Schreiber ESG, Forsyth DM, Choquenot D, Clancy TF (2005) Factors affecting grey-headed flying fox (Pteropus poliocephalus: Pteropodidae) foraging in the Melbourne metropolitan area, Australia. Aust Ecol 30:600–608
Mickleburgh SP, Hutson AM, Racey PA (1992) Old world fruit bats: an action plan for their conservation. IUCN/SSC chiroptera specialist group report. IUCN, Gland, Switzerland
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
O’Ryan C, Harley EH, Bruford MW, Beaumont M, Wayne RK, Cherry MI (1998) Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Anim Conserv 1:85–94
Petri B, Pääbo S, Von Haeseler A, Tautz D (1997) Paternity assessment and population subdivision in a natural population of the larger mouse-eared bat Myotis myotis. Mol Ecol 6:235–242
Pimm SL, Gittleman JL, McCracken GF, Gilpin ME (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol Evol 4:176–178
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reduction in the effective population size using allele frequency data. J Hered 90:502–503
Powell VJ, Wehnelt SC (2003) A new estimate of the population size of the critically endangered Rodrigues fruit bat Pteropus rodricensis. Oryx 37:353–357
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 2:185–193
Raymond M, Rousset F (2000) GENEPOP Version 3.2: an updated, version of GENEPOP (Version 1.2), population genetics software for exact tests and ecumenism. J Hered 86:248–249
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Ryder OA (1986) Genetic investigations: tools for supporting breeding programme goals. Int Zoo Yearbook 24/25:157–162
Schneider S, Kueffer J-M, Roessli D, Excoffier L (1997) Arlequin ver.1.1, A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland
Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioural sciences. McGraw-Hill Co., New York
Simberloff D (1988) The contribution of population and community biology to conservation science. Annu Rev Ecol Syst 19:473–511
Soulé ME (1983) What do we really know about extinction? In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas L (eds) Genetics and conservation. Benjamin Cummings Publishing Company, London, UK, pp 111–124
Stockley P, Searle JB, MacDonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond, B 254:173–179
Storz JF (2000) Variation at tri- and tetranucleotide repeat microsatellite loci in the fruit bat genus Cynopterus (Chiroptera: Pteropodidae). Mol Ecol 9:2155–2234
Storz JF, Bhat HR, Kunz TH (2001a) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. I. Inbreeding, outbreeding, and population subdivision. Evolution 55:1215–1223
Storz JF, Bhat HR, Kunz TH (2001b) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. II. Variance in male mating success and effective population size. Evolution 55:1224–1232
Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchial Bayesian model. Evolution 56:154–166
Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Weishampel JF (1990) Maintaining genetic variation in a one-way two island model. J Wildl Manage 54:676–682
Whitman KL (1998) Control region sequence divergence within and between wild and captive populations of Rodrigues fruit bats (Pteropus rodricensis): implications for conservation and management. Unpublished Masters thesis, Villanova University, USA
Worthington-Wilmer J, Barrett E (1996) A non-lethal method of sampling for genetic studies of chiropterans. Bat Res News 37:1–3
Zenger KR, Richardson BJ, Vachot-Griffin A-M (2003) A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12:789–794
Acknowledgements
We thank Dublin Zoo for funding this project, Enterprise Ireland for a research grant to JOB (Grant No.: BR/2001/226) and The Lubee Bat Conservancy for a grant to GFM for development of microsatellite markers. Additional thanks to the staff of Dublin Zoo for assisting in the collection of skin samples and to V. Powell (Manchester Metropolitan University) and V. Tataya (Mauritian Wildlife Foundation) for skin samples from Rodrigues Island. D. Doyle, J. Carolan, and L. Bailey provided technical assistance and S. Mariani provided useful comments on an earlier draft of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
O’Brien, J., McCracken, G.F., Say, L. et al. Rodrigues fruit bats (Pteropus rodricensis, Megachiroptera: Pteropodidae) retain genetic diversity despite population declines and founder events. Conserv Genet 8, 1073–1082 (2007). https://doi.org/10.1007/s10592-006-9263-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-006-9263-1