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Conservation Genetics

, Volume 15, Issue 2, pp 245–260 | Cite as

Fragmentation genetics of rainforest animals: insights from recent studies

  • U. RadespielEmail author
  • M. W. Bruford
Review Article

Abstract

Habitat fragmentation is one of the most prominent effects of anthropogenic ecosystem degradation. However, despite the accumulating evidence that anthropogenic habitat fragmentation acts negatively on the dynamics and viability of many species, rainforest fragmentation can occur naturally. The need to disentangle ‘natural’ fragmentation processes from (often) very recent anthropogenic effects poses a methodological challenge in the field of conservation genetics. Additional challenges include sampling schemes that can generate false signals of population size changes or population genetic structure. Finally, limited analytical power often results from restricted sample sizes, numbers of markers, or their informativeness. We reviewed the available literature on the effects of habitat fragmentation in non-aquatic tropical animal species over the last 10 years to ask what has been learned as a result of the increasing attention paid to these methodological issues. Fifty-four studies contained relevant datasets on the question of fragmentation effects in 74 animal species. Primates (n = 18) and passerine birds (n = 17) contributed most species to the survey. Unambiguous signals of fragmentation effects were reported in 33.8 % of species, whereas the remaining species showed either equivocal (36.5 %) or no evidence (29.7 %) of fragmentation effects. Our review further reveals that uneven sampling cannot be ruled out as possible explanation for many of the reported genetic bottleneck signals and genetic structure effects. Based on the reviewed evidence, methodological (e.g. improving sampling schemes, multiple analytical approaches, added value of different markers) and conceptual recommendations offering a better understanding of general and species-specific evolutionary responses to fragmentation are formulated for future studies.

Keywords

Habitat loss Sampling effects Genetic bottleneck Genetic diversity Genetic structure Statistical power 

Notes

Acknowledgments

We thank the organizers (Dr. Chris Kettle and Aline Finger) of the gtö symposium 2012 in Erlangen/Germany on “Fragmentation Effects in the Tropics” for the invitation to contribute this review to this special issue of Conservation Genetics. UR acknowledges the continuous support of the Institute of Zoology, TiHo Hannover and in particular Elke Zimmermann. MWB acknowledges the Royal Society, Cardiff University, the Leverhulme Trust and Darwin Initiative for financial support for tropical fragmentation studies and their dissemination. Finally, thanks go to two anonymous reviewers for their comments that helped to improve the manuscript considerably.

References

  1. Achard F, Eva HD, Stibig HJ, Mayaux P, Gallego J, Richards T, Malingreau JP (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297:999–1002PubMedCrossRefGoogle Scholar
  2. Barnett J, Ruiz-Gutierrez V, Coulon A, Lovette I (2008) Weak genetic structuring indicates ongoing gene flow across white-ruffed manakin (Corapipo altera) populations in a highly fragmented Costa Rica landscape. Conserv Genet 9:1403–1412CrossRefGoogle Scholar
  3. Bergl RA, Vigilant L (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the cross river gorilla (Gorilla gorilla diehli). Mol Ecol 16:501–516PubMedCrossRefGoogle Scholar
  4. Blair ME, Melnick DJ (2012) Scale-dependent effects of a heterogeneous landscape on genetic differentiation in the Central American squirrel monkey (Saimiri oerstedii). PLoS ONE 7:e43027PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bowyer J, Newell G, Eldridge MB (2002) Genetic effects of habitat contraction on Lumholtz’s tree-kangaroo (Dendrolagus lumholtzi) in the Australian wet tropics. Conserv Genet 3:61–67CrossRefGoogle Scholar
  6. Brooks TM, Mittermeier RA, da Fonseca GAB, Gerlach J, Hoffmann M, Lamoreux JF, Mittermeier CG, Pilgrim JD, Rodrigues ASL (2006) Global biodiversity conservation priorities. Science 313:58–61PubMedCrossRefGoogle Scholar
  7. Brown L, Ramey R, Tamburini B, Gavin T (2004) Population structure and mitochondrial DNA variation in sedentary neotropical birds isolated by forest fragmentation. Conserv Genet 5:743–757CrossRefGoogle Scholar
  8. Callens TOM, Galbusera P, Matthysen E, Durand EY, Githiru M, Huyghe JR, Lens LUC (2011) Genetic signature of population fragmentation varies with mobility in seven bird species of a fragmented Kenyan cloud forest. Mol Ecol 20:1829–1844PubMedCrossRefGoogle Scholar
  9. Chaves PB, Alvarenga CS, Possamai CB, Dias LG, Boubli JP, Strier KB, Mendes SL, Fagundes V (2011) Genetic diversity and population history of a critically endangered primate, the Northern muriqui (Brachyteles hypoxanthus). PLoS ONE 6:e20722PubMedCentralPubMedCrossRefGoogle Scholar
  10. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995PubMedCentralPubMedCrossRefGoogle Scholar
  11. Chu J-H, Lin Y-S, Wu H-Y (2005) Mitochondrial DNA diversity in two populations of Taiwanese macaque (Macaca cyclopis). Conserv Genet 6:101–109CrossRefGoogle Scholar
  12. Ciofi C, Beaumont MA, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the komodo dragon Varanus komodoensis. Proc R Soc Lond B 266:2269–2274CrossRefGoogle Scholar
  13. Craul M, Chikhi L, Sousa V, Olivieri GL, Rabesandratana A, Zimmermann E, Radespiel U (2009) Influence of forest fragmentation on an endangered large-bodied lemur in Northwestern Madagascar. Biol Conserv 142:2862–2871CrossRefGoogle Scholar
  14. Cushman SA, Shirk A, Landguth EL (2012) Separating the effects of habitat area, fragmentation and matrix resistance on genetic differentiation in complex landscapes. Landsc Ecol 27:369–380CrossRefGoogle Scholar
  15. de Thoisy B, Hrbek T, Farias IP, Vasconcelos WR, Lavergne A (2006) Genetic structure, population dynamics, and conservation of black caiman (Melanosuchus niger). Biol Conserv 133:474–482CrossRefGoogle Scholar
  16. Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian atlantic coastal forest. Biol Conserv 142:1560–1569CrossRefGoogle Scholar
  17. England PR, Luikart G, Waples RS (2010) Early detection of population fragmentation using linkage disequilibrium estimation of effective population size. Conserv Genet 11:2425–2430CrossRefGoogle Scholar
  18. Ernest EM, Haanes H, Bitanyi S, Fyumagwa RD, Msoffe PL, Bjørnstad G, Røed KH (2012) Influence of habitat fragmentation on the genetic structure of large mammals: evidence for increased structuring of African buffalo (Syncerus caffer) within the Serengeti ecosystem. Conserv Genet 13:381–391CrossRefGoogle Scholar
  19. Frankel OH, Soulé ME (1981) Conserv Evol. Cambridge University Press, CambridgeGoogle Scholar
  20. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  21. Freedman AH, Thomassen HA, Buermann W, Smith TB (2010) Genomic signals of diversification along ecological gradients in a tropical lizard. Mol Ecol 19:3773–3788PubMedCrossRefGoogle Scholar
  22. Funk S, Fa J (2006) Phylogeography of the endemic St. Lucia whiptail lizard Cnemidophorus vanzoi: conservation genetics at the species boundary. Conserv Genet 7:651–663CrossRefGoogle Scholar
  23. Galbusera P, Githiru M, Lens L, Matthysen E (2004) Genetic equilibrium despite habitat fragmentation in an Afrotropical bird. Mol Ecol 13:1409–1421PubMedCrossRefGoogle Scholar
  24. Gebremedhin B, Ficetola GF, Naderi S, Rezaei HR, Maudet C, Rioux D, Luikart G, Flagstad Ø, Thuiller W, Taberlet P (2009) Combining genetic and ecological data to assess the conservation status of the endangered Ethiopian walia ibex. Anim Cons 12:89–100CrossRefGoogle Scholar
  25. Girod C, Vitalis R, Leblois R, Fréville H (2011) Inferring population decline and expansion from microsatellite data: a simulation evaluation of the Msvar method. Genetics 188:166–179CrossRefGoogle Scholar
  26. Goossens B, Chikhi L, Jalil MF, Ancrenaz M, Lackman-Ancrenaz I, Mohamed M, Andau P, Bruford MW (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol Ecol 14:441–456PubMedCrossRefGoogle Scholar
  27. Goossens B, Chikhi L, Ancrenaz M, Lackman-Ancrenaz I, Andau P, Bruford MW (2006) Genetic signature of anthropogenic population collapse in orang-utans. PLoS Biol 4:285–291CrossRefGoogle Scholar
  28. Gottelli D, Marino J, Sillero-Zubiri C, Funk SM (2004) The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Mol Ecol 13:2275–2286PubMedCrossRefGoogle Scholar
  29. Gottelli D, Sillero-Zubiri C, Marino J, Funk SM, Wang J (2013) Genetic structure and patterns of gene flow among populations of the endangered Ethiopian wolf. Anim Cons 16:234–247CrossRefGoogle Scholar
  30. Guschanski K, Olivieri G, Funk SM, Radespiel U (2007) MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis. Conserv Genet 8:809–821CrossRefGoogle Scholar
  31. Haag CR, Saastamoinen M, Marden JH, Hanski I (2005) A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc R Soc Lond B 272:2449–2456CrossRefGoogle Scholar
  32. Haag T, Santos AS, Sana DA, Morato RG, Cullen L Jr, Crawshaw PG Jr, De Angelo C, Di Bitetti MS, Salzano FM, Eizirik E (2010) The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of atlantic forest jaguars (Panthera onca). Mol Ecol 19:4906–4921PubMedCrossRefGoogle Scholar
  33. Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137PubMedCrossRefGoogle Scholar
  34. Harley EH, Baumgarten I, Cunningham J, O’Ryan C (2005) Genetic variation and population structure in remnant populations of black rhinoceros, Diceros bicornis, in Africa. Mol Ecol 14:2981–2990PubMedCrossRefGoogle Scholar
  35. Heller R, Okello JBA, Siegismund H (2010) Can small wildlife conservancies maintain genetically stable populations of large mammals? Evidence for increased genetic drift in geographically restricted populations of cape buffalo in East Africa. Mol Ecol 19:1324–1334PubMedCrossRefGoogle Scholar
  36. Hirota M, Holmgren M, Van Nes EH, Scheffer M (2011) Global resilience of tropical forest and savanna to critical transitions. Science 334:232–235PubMedCrossRefGoogle Scholar
  37. Hoban SM, Gaggiotti OE, Bertorelle G (2013a) The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Mol Ecol 22(13):3444–3450PubMedCrossRefGoogle Scholar
  38. Hoban S, Gaggiotti O, the Congress Consortium, Bertorelle G (2013b) Sample planning optimization tool for conservation and population Genetics (SPOTG): a software for choosing the appropriate number of markers and samples. Methods Ecol Evol 4(3):299–303. doi: 10.1111/2041-210x.12025 CrossRefGoogle Scholar
  39. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485PubMedCrossRefGoogle Scholar
  40. Keyghobadi NKN (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064CrossRefGoogle Scholar
  41. Koh LP, Sodhi NS (2010) Conserving Southeast Asia’s imperiled biodiversity: scientific, management, and policy challenges. Biodiv Conserv 19:913–917CrossRefGoogle Scholar
  42. Landguth EL, Balkenhol N (2012) Relative sensitivity of neutral versus adaptive genetic data for assessing population differentiation. Conserv Genet 13:1421–1426CrossRefGoogle Scholar
  43. Landguth EL, Fedy BC, Oyler-McCance SJ, Garey AL, Emel SL, Mumma M, Wagner HH, Fortin M-J, Cushman SA (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol Ecol Res 12:276–284CrossRefGoogle Scholar
  44. Lara-Ruiz P, Chiarello AG, Santos FR (2008) Extreme population divergence and conservation implications for the rare endangered atlantic forest sloth, Bradypus torquatus (Pilosa: Bradypodidae). Biol Conserv 141:1332–1342CrossRefGoogle Scholar
  45. Laurance WF, Delamônica P, Laurance SG, Vasconcelos HL, Lovejoy TE (2000) Rainforest fragmentation kills big trees. Nature 404:836PubMedCrossRefGoogle Scholar
  46. Laurance WF et al (2012) Averting biodiversity collapse in tropical forest protected areas. Nature 489:290–294PubMedCrossRefGoogle Scholar
  47. Lawler R (2011) Historical demography of a wild lemur population (Propithecus verreauxi) in southwest Madagascar. Popul Ecol 53:229–240CrossRefGoogle Scholar
  48. Leigh K, Zenger K, Tammen I, Raadsma H (2012) Loss of genetic diversity in an outbreeding species: small population effects in the African wild dog (Lycaon pictus). Conserv Genet 13:767–777CrossRefGoogle Scholar
  49. Lerner HRL, Johnson JA, Lindsay AR, Kiff LF, Mindell DP (2009) It’s not too late for the harpy eagle (Harpia harpyja): high levels of genetic diversity and differentiation can fuel conservation programs. PLoS ONE 4:e7336PubMedCentralPubMedCrossRefGoogle Scholar
  50. Louis EE, Ratsimbazafy JH, Razakamaharauo VR, Pierson DJ, Barber RC, Brenneman RA (2005) Conservation genetics of black and white ruffed lemurs, Varecia variegata, from Southeastern Madagascar. Anim Cons 8:105–111CrossRefGoogle Scholar
  51. Lynch M, Conery J, Burger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518CrossRefGoogle Scholar
  52. Malone C, Knapp C, Taylor J, Davis S (2003) Genetic consequences of pleistocene fragmentation: isolation, drift, and loss of diversity in rock iguanas (Cyclura). Conserv Genet 4:1–15CrossRefGoogle Scholar
  53. Mbora DM, McPeek M (2010) Endangered species in small habitat patches can possess high genetic diversity: the case of the Tana River red colobus and mangabey. Conserv Genet 11:1725–1735CrossRefGoogle Scholar
  54. Measey GJ, Galbusera P, Breyne P, Matthysen E (2007) Gene flow in a direct-developing, leaf litter frog between isolated mountains in the Taita Hills, Kenya. Conserv Genet 8:1177–1188CrossRefGoogle Scholar
  55. Milton K, Lozier J, Lacey E (2009) Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Conserv Genet 10:347–358CrossRefGoogle Scholar
  56. Mixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian atlantic coastal forest. Biol Conserv 142:1560–1569CrossRefGoogle Scholar
  57. Nason JD, Hamrick JL (1997) Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees. J Hered 88:264–276CrossRefGoogle Scholar
  58. Nazareno AG, Jump AS (2012) Species–genetic diversity correlations in habitat fragmentation can be biased by small sample sizes. Mol Ecol 21:2847–2849PubMedCrossRefGoogle Scholar
  59. Nielsen R, Beaumont MA (2009) Statistical inferences in phylogeography. Mol Ecol 18:1034–1047PubMedCrossRefGoogle Scholar
  60. Norton JE, Ashley MV (2004) Genetic variability and population structure among wild Baird’s tapirs. Anim Cons 7:211–220CrossRefGoogle Scholar
  61. Oliveras de Ita A, Oyama K, Smith T, Wayne R, Milá B (2012) Genetic evidence for recent range fragmentation and severely restricted dispersal in the critically endangered Sierra Madre sparrow, Xenospiza baileyi. Conserv Genet 13:283–291CrossRefGoogle Scholar
  62. Olivieri GL, Sousa V, Chikhi L, Radespiel U (2008) From genetic diversity and structure to conservation: genetic signature of recent population declines in three mouse lemur species (Microcebus spp.). Biol Conserv 141:1257–1271CrossRefGoogle Scholar
  63. Ottewell K, Grey E, Castillo F, Karubian J (2012) The pollen dispersal kernel and mating system of an insect-pollinated tropical palm Oenocarpus bataua. Heredity 109:332–339PubMedCentralPubMedCrossRefGoogle Scholar
  64. Pavlova A, Walker F, Ree R, Cesarini S, Taylor A (2010) Threatened populations of the Australian squirrel glider (Petaurus norfolcensis) show evidence of evolutionary distinctiveness on a late pleistocene timescale. Conserv Genet 11:2393–2407CrossRefGoogle Scholar
  65. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418PubMedCrossRefGoogle Scholar
  66. Pérez-Espona S, McLeod JE, Franks NR (2012) Landscape genetics of a top neotropical predator. Mol Ecol 21:5969–5985PubMedCrossRefGoogle Scholar
  67. Peter BM, Wegmann D, Excoffier L (2010) Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol Ecol 19:4648–4660PubMedCrossRefGoogle Scholar
  68. Potter S, Eldridge MB, Cooper SB, Paplinska J, Taggart D (2012) Habitat connectivity, more than species’ biology, influences genetic differentiation in a habitat specialist, the short-eared rock-wallaby (Petrogale brachyotis). Conserv Genet 13:937–952CrossRefGoogle Scholar
  69. Quéméré E, Crouau-Roy B, Rabarivola C, Louis EE Jr, Chikhi L (2010a) Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range. Mol Ecol 19:1606–1621PubMedCrossRefGoogle Scholar
  70. Quéméré E, Louis E Jr, Ribéron A, Chikhi L, Crouau-Roy B (2010b) Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range. Conserv Genet 11:675–687CrossRefGoogle Scholar
  71. Quéméré E, Amelot X, Pierson J, Crouau-Roy B, Chikhi L (2012) Genetic data suggest a natural prehuman origin of open habitats in Northern Madagascar and question the deforestation narrative in this region. Proc Natl Acad Sci USA 109:13018–13033CrossRefGoogle Scholar
  72. Reddy PA, Gour DS, Bhavanishankar M, Jaggi K, Hussain SM, Harika K, Shivaji S (2012) Genetic evidence of tiger population structure and migration within an isolated and fragmented landscape in Northwest India. PLoS ONE 7:e29827PubMedCentralPubMedCrossRefGoogle Scholar
  73. Reding D, Freed L, Cann R, Fleischer R (2010) Spatial and temporal patterns of genetic diversity in an endangered Hawaiian honeycreeper, the Hawaii Akepa (Loxops coccineus coccineus). Conserv Genet 11:225–240CrossRefGoogle Scholar
  74. Rodriguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Res 12:873–884CrossRefGoogle Scholar
  75. Rossetto M, Jones R, Hunter J (2004) Genetic effects of rainforest fragmentation in an early successional tree (Elaeocarpus grandis). Heredity 93:610–618PubMedCrossRefGoogle Scholar
  76. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  77. Schad J, Sommer S, Ganzhorn JU (2004) MHC variability of a small lemur in the littoral forest fragments of Southeastern Madagascar. Conserv Genet 5:299–309CrossRefGoogle Scholar
  78. Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452CrossRefGoogle Scholar
  79. Sharma R, Arora N, Goossens B, Nater A, Morf N, Salmona J, Bruford MW, Van Schaik CP, Krützen M, Chikhi L (2012) Effective population size dynamics and the demographic collapse of Bornean orang-utans. PLoS ONE 7:e49429PubMedCentralPubMedCrossRefGoogle Scholar
  80. Smith TB, Wayne RK, Girman DJ, Bruford MW (1997) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857CrossRefGoogle Scholar
  81. Sommer S (2003) Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 12:2845–2851PubMedCrossRefGoogle Scholar
  82. Struebig MJ, Kingston T, Petit EJ, Le Comber SC, Zubaid A, Mohd-Adnan A, Rossiter SJ (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecol Lett 14:582–590PubMedCrossRefGoogle Scholar
  83. Sumner J (2005) Decreased relatedness between male prickly forest skinks (Gnypetoscincus queenslandiae) in habitat fragments. Conserv Genet 6:333–340CrossRefGoogle Scholar
  84. Sumner J, Jessop T, Paetkau D, Moritz C (2004) Limited effect of anthropogenic habitat fragmentation on molecular diversity in a rain forest skink, Gnypetoscincus queenslandiae. Mol Ecol 13:259–269PubMedCrossRefGoogle Scholar
  85. Sunnocks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203CrossRefGoogle Scholar
  86. Telles MPC, Diniz-Filho JAF, Bastos RP, Soares TN, Guimarães LDA, Lima LP (2007) Landscape genetics of Physalaemus cuvieri in Brazilian Cerrado: correspondence between population structure and patterns of human occupation and habitat loss. Biol Conserv 139:37–46CrossRefGoogle Scholar
  87. Tscharntke T, Steffan-Dewenter I, Kreuss A, Thies C (2002) Contribution of small habitat fragments to conservation of insect communities of grassland–cropland landscapes. Ecol Apps 12:354–363Google Scholar
  88. Van Treuren R, Bijlsma R, Van Delden W, Ouborg NJ (1990) The significance of genetic erosion in the process of extinction 1. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66:181–189CrossRefGoogle Scholar
  89. van Vuuren BJ, Woolaver L, Goodman SM (2012) Genetic population structure in the boky–boky (Carnivora: Eupleridae), a conservation flagship species in the dry deciduous forests of central Western Madagascar. Anim Cons 15:164–173CrossRefGoogle Scholar
  90. Vandergast AG, Gillespie RG, Roderick GK (2004) Influence of volcanic activity on the population genetic structure of Hawaiian Tetragnatha spiders: fragmentation, rapid population growth and the potential for accelerated evolution. Mol Ecol 13:1729–1743PubMedCrossRefGoogle Scholar
  91. VanderWerf E, Young L, Yeung N, Carlon D (2010) Stepping stone speciation in Hawaii’s flycatchers: molecular divergence supports new island endemics within the elepaio. Conserv Genet 11:1283–1298CrossRefGoogle Scholar
  92. Vellend M (2004) Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85:3043–3055CrossRefGoogle Scholar
  93. Vidya TNC, Varma S, Dang N, Thanh T, Sukumar R (2007) Minimum population size, genetic diversity, and social structure of the Asian elephant in Cat Tien National Park and its adjoining areas, Vietnam, based on molecular genetic analyses. Conserv Genet 8:1471–1478CrossRefGoogle Scholar
  94. Wheat CW (2010) Phosphoglucose isomerase (Pgi) performance and fitness effects among Arthropods and its potential role as an adaptive marker in conservation genetics. Conserv Genet 11:387–397CrossRefGoogle Scholar
  95. Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST ≠ 1/(4Nm + 1). Heredity 82:117–125PubMedCrossRefGoogle Scholar
  96. Woltmann S, Kreiser B, Sherry T (2012) Fine-scale genetic population structure of an understory rainforest bird in Costa Rica. Conserv Genet 13:925–935CrossRefGoogle Scholar
  97. Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of populations inside protected areas. Science 280:2126–2128PubMedCrossRefGoogle Scholar
  98. Wright TF, Rodriguez AM, Fleischer RC (2005) Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata. Mol Ecol 14:1197–1205PubMedCrossRefGoogle Scholar
  99. Zimmermann Y, Schorkopf DLP, Moritz RFA, Pemberton RW, Quezada-Euan JJG, Eltz T (2011) Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conserv Genet 12:1183–1194CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of ZoologyUniversity of Veterinary Medicine HanoverHannoverGermany
  2. 2.Cardiff School of BiosciencesCardiff UniversityCardiffUK

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