Skip to main content

Crumbling diversity: comparison of historical archived and contemporary natural populations indicate reduced genetic diversity and increasing genetic differentiation in the golden-cheeked warbler

Abstract

Genetic viability of threatened and endangered species is of increasing concern with habitat loss and fragmentation. Valuable assessments of the genetic status of endangered species are difficult in most cases, where only single sample estimates are available. Using historical and contemporary samples, we assessed the impact of both historical and recent demographic changes on population genetics of the endangered golden-cheeked warbler, (Dendroica chrysoparia). Our study documents a steep decline in genetic diversity in an endangered species over a 100-year period, along with concurrent increase in genetic differentiation, and low contemporary effective sizes for all the populations we evaluated. While adding to the growing body of literature that describes the genetic impacts of habitat fragmentation, our study may also serve as an informative guide to future management of endangered species. Our study underlines the importance of long term population genetic monitoring in understanding the full extent of genetic changes in endangered species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Alo D, Turner TF (2005) Effects of habitat fragmentation on effective population size in the endangered Rio Grande silvery minnow. Conserv Biol 19:1138–1148

    Article  Google Scholar 

  • Angelone S, Holderegger R (2009) Population genetics suggests effectiveness of habitat connectivity measures for the European tree frog in Switzerland. J Appl Ecol 46:879–887

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chiki L, Raufaste N, Bonhomme F (2004) Genetix 4.05. logiciel sous windows TM pour la genetique des populations. Laboratoire genome, populations, interactions, CNRS UMR 5000. Universite de Montpellier II, Montpellier

    Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    Article  PubMed  CAS  Google Scholar 

  • Born C, Hardy OJ, Chevallier MH, Ossari S, Atteke C, Wickings J, Hossaert-Mckey M (2008) Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Mol Ecol 17:2041–2050

    Article  PubMed  Google Scholar 

  • Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2008) Temporal changes in allele frequencies but stable genetic diversity over the past 40 years in the Irish sea population of Thornback ray, raja clavata. Heredity 101:120–126

    Article  PubMed  CAS  Google Scholar 

  • Crow JF, Denniston C (1988) Inbreeding and variance effective population numbers. Evolution 42:482–495

    Article  Google Scholar 

  • 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 142:1560–1569

    Article  Google Scholar 

  • Ellegren H (1991) DNA typing of museum birds. Nature 354:113

    Article  PubMed  CAS  Google Scholar 

  • Ellis JS, Knight ME, Darvill B, Goulson D (2006) Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol Ecol 15:4375–4386

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995b) Effective population-size adult-population size ratios in wildlife—a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R (1995c) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–800

    Article  Google Scholar 

  • Frels D Jr (2006) Performance report. Kerr Wildlife Management Area, Hunt, p 8

    Google Scholar 

  • Goudet J (2002) FSTAT 2.9.3.2, a program to estimate and test gene diversities and fixation indices. http://www.unil.ch/izea/softwares/fstat.html. Accessed 25 April 2010

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  • Howeth JG, McGaugh SE, Hendrickson DA (2008) Contrasting demographic and genetic estimates of dispersal in the endangered coahuilan box turtle: a contemporary approach to conservation. Mol Ecol 17:4209–4221

    Article  PubMed  Google Scholar 

  • Jordan MA, Snell HL (2008) Historical fragmentation of islands and genetic drift in populations of galapagos lava lizards (Microlophus albemarlensis complex). Mol Ecol 17:1224–1237

    Article  PubMed  CAS  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885

    Article  PubMed  Google Scholar 

  • Kroll JC (1980) Habitat requirements of the golden-cheeked warbler: management implications. J Range Manag 33:60–66

    Article  Google Scholar 

  • Lage C, Kornfield I (2006) Reduced genetic diversity and effective population size in an endangered Atlantic salmon (Salmo salar) population from Maine, USA. Conserv Genet 7:91–104

    Article  Google Scholar 

  • Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477–494

    Article  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: Effects of sample size and bottlenecks. Mol Ecol 11:2445–2451

    Article  PubMed  CAS  Google Scholar 

  • Leberg PL, Athrey GNR, Barr KR, Lindsay D, Lance R (2009) Implications of landscape alteration for the conservation of genetic diversity of endangered species. In: DeWoody JA, Bickham JW, Michler C, Nichols K, Rhodes OE, Woeste K (eds) Molecular insights into natural resource conservation and management. Cambridge University Press, Cambridge, p 392

    Google Scholar 

  • Lindsay DL, Barr KR, Lance R, Tweddale SA, Hayden TJ, Leberg PL (2008) Habitat fragmentation and genetic diversity of an endangered, migratory songbird, the golden-cheeked warbler (Dendroica chrysoparia). Mol Ecol 17:2122–2133

    Article  PubMed  Google Scholar 

  • Martinez-Cruz B, Godoy JA, Negro JJ (2007) Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Mol Ecol 16:477–486

    Article  PubMed  CAS  Google Scholar 

  • Miller CR, Joyce P, Waits LP (2002) Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160:357–366

    PubMed  Google Scholar 

  • Nei M, Tajima F (1981) Genetic drift and estimation of effective population-size. Genetics 98:625–640

    PubMed  CAS  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Nichols RA, Bruford MW, Groombridge JJ (2001) Sustaining genetic variation in a small population: evidence from the mauritius kestrel. Mol Ecol 10:593–602

    Article  PubMed  CAS  Google Scholar 

  • Nunney L (1995) Measuring the ratio of effective population-size to adult numbers using genetic and ecological data. Evolution 49:389–392

    Article  Google Scholar 

  • Nunney L (2000) The limits to knowledge in conservation genetics—the value of effective population size. J Evolut Biol 32:179–194

    Article  Google Scholar 

  • Peak RG (2007) Forest edges negatively affect golden-cheeked warbler nest survival. Condor 109:628–637

    Article  Google Scholar 

  • Rappole JH, King DI, Diez J (2003) Winter- vs. breeding-habitat limitation for an endangered avian migrant. Ecol Appl 13:735–742

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reidy JL, Thompson FR, Peak RG (2009) Factors affecting golden-cheeked warbler nest survival in urban and rural landscapes. J Wildl Manag 73:407–413

    Article  Google Scholar 

  • Rodriguez-Munoz R, Mirol PM, Segelbacher G, Fernandez A, Tregenza T (2007) Genetic differentiation of an endangered capercaillie (Tetrao urogallus) population at the southern edge of the species range. Conserv Genet 8:659–670

    Article  Google Scholar 

  • Sato T, Harada Y (2008) Loss of genetic variation and effective population size of Kirikuchi charr: implications for the management of small, isolated salmonid populations. Anim Conserv 11:153–159

    Article  Google Scholar 

  • Schmidly DJ, Sansom A (2002) Texas natural history: a century of change, 1st edn. Texas Tech University, Lubbock

    Google Scholar 

  • Segelbacher G, Manel S, Tomiuk J (2008) Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus). Mol Ecol 17:2356–2367

    Article  PubMed  CAS  Google Scholar 

  • Sperry JH, Peak RG, Cimprich DA, Weatherhead PJ (2008) Snake activity affects seasonal variation in nest predation risk for birds. J Avian Biol 39:379–383

    Article  Google Scholar 

  • USFWS (1992) Golden-cheeked warbler (Dendroica chrysoparia) recovery plan. U.S. Fish and Wildlife, Albuqurque, p 97

    Google Scholar 

  • USFWS (2004) Biological opinion, consultation number: 2-12-05-F-021. U.S. Fish and Wildlife Service, Pennsylvania

  • Valiére N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379

    Google Scholar 

  • 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 4:535–538

    Article  Google Scholar 

  • Veit ML, Robertson RJ, Hamel PB, Friesen VL (2005) Population genetic structure and dispersal across a fragmented landscape in cerulean warblers (Dendroica cerulea). Conserv Genet 6:159–174

    Article  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    PubMed  CAS  Google Scholar 

  • Yamamoto S, Morita K, Koizumi I, Maekawa K (2004) Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial-temporal changes in gene frequencies. Conserv Genet 5:529–538

    Article  CAS  Google Scholar 

  • Young A, Clarke GM (2000) Conclusions and future directions: what do we know about the genetic and demographic effects of habitat fragmentation and where do we go from here? In: Young A, Clarke GM (eds) Genetics, demography and viability of fragmented populations, 1st edn. Cambridge University Press, Cambridge, pp 361–366

    Chapter  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  PubMed  CAS  Google Scholar 

  • Zartman CE, McDaniel SF, Shaw AJ (2006) Experimental habitat fragmentation increases linkage disequilibrium but does not affect genetic diversity or population structure in the Amazonian liverwort Radula flaccida. Mol Ecol 15:2305–2315

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the AMNH, New York, NY, MCZ Harvard University, Cambridge, MA, FMNH, Chicago, IL, and NMNH, Washington DC for tissue samples. We thank Ft. Hood, Kerr WMA, Balcones Canyonlands NWR, TPWD, K. Barr, C. Goates, J. Hernandez, S. Pathikonda, and L. Butler for access to field sites, and help with field sampling. We thank J. Neigel, S. Mopper and D. Johnson and anonymous reviewers for comments on an earlier version of this manuscript. This study was funded by U.S. Department of Defense under the Section 6.1 Basic Research Program and U.S. Army 6.2 Threatened and Endangered Species Program to RFL and PLL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giridhar Athrey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Appendices

Appendix 1

See Tables 4, 5, 6 and 7

Table 4 Historical population summary of diversity indices
Table 5 Nei’s estimation of heterozygosity
Table 6 Modern population’s summary of diversity
Table 7 Diversity measures

Appendix 2

 

Sample ID

Museum

A382291

AMNH

A382292

AMNH

A382293

AMNH

A382294

AMNH

A382295

AMNH

A382296

AMNH

A382297

AMNH

A382360

AMNH

A382361

AMNH

A382362

AMNH

A382363

AMNH

A382364

AMNH

A382365

AMNH

A382305

AMNH

A382310

AMNH

A382313

AMNH

A382318

AMNH

A382323

AMNH

A382327

AMNH

A382329

AMNH

A382335

AMNH

A382340

AMNH

A382341

AMNH

A382346

AMNH

A382348

AMNH

A382351

AMNH

A382352

AMNH

A507004

AMNH

F149870

FMNH

F149871

FMNH

F149872

FMNH

F26172

FMNH

F308240

FMNH

F308244

FMNH

M101045

MCZ

M101254

MCZ

M204935

MCZ

M214364

MCZ

M28413

MCZ

M326084

MCZ

M326086

MCZ

M320914

MCZ

M320923

MCZ

M320940

MCZ

M320941

MCZ

M320943

MCZ

M320946

MCZ

M320956

MCZ

M320957

MCZ

M320964

MCZ

M320965

MCZ

M320967

MCZ

M320968

MCZ

M320971

MCZ

M382341

MCZ

M382364

MCZ

M382380

MCZ

N141771

NMNH

N152408

NMNH

N592677

NMNH

N133176

NMNH

N150528

NMNH

N152520

NMNH

N152527

NMNH

N153056

NMNH

N153057

NMNH

N181808

NMNH

N184442

NMNH

N184833

NMNH

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Athrey, G., Lindsay, D.L., Lance, R.F. et al. Crumbling diversity: comparison of historical archived and contemporary natural populations indicate reduced genetic diversity and increasing genetic differentiation in the golden-cheeked warbler. Conserv Genet 12, 1345–1355 (2011). https://doi.org/10.1007/s10592-011-0235-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-011-0235-8

Keywords

  • Genetic diversity
  • Fragmentation
  • Effective population size
  • Endangered birds
  • Historical-contemporary samples