Advertisement

Predicting population extinctions in Darwin’s finches

  • Heather L. FarringtonEmail author
  • Lucinda P. Lawson
  • Kenneth Petren
Research Article
  • 44 Downloads

Abstract

Genetic data are increasingly used for fast, efficient, and cost-effective monitoring of natural populations and assessment of extinction risk in species management. A single modern molecular snapshot is typically used to infer population size and vulnerability, yet for species with unknown and potentially complex genetic metapopulation structure, this technique may not effectively predict vulnerability. Darwin’s finches, which are well-represented in museum collections, offer a unique opportunity to test the effectiveness of predicting extinction vulnerability in species with complex structure, such as naturally fragmented populations. In this study, we compared ancient DNA from ~ 100 year old extinct and extant Darwin’s finch populations in the Galápagos Islands to determine whether single time point genetic assessments in the past accurately predicted extinction risk, or if other factors such as metapopulation dynamics could mask population declines. Of eight extinct populations, only one had significantly reduced genetic variation compared to an extant population of similar characteristics. Contrary to our prediction that populations would have decreased genetic diversity prior to extinction when compared to persisting populations, at least one measure of genetic diversity was significantly higher in six of the eight extinct populations when compared to extant populations. Simulations lend support to the hypothesis that unaccounted for metapopulation structure may explain the observed pattern in many species. Therefore, models of genetic diversity reflecting population extinction potential may be inadequate for highly-mobile species with metapopulation dynamics such as the Galápagos finches.

Keywords

Extinction risk Metapopulation dynamics Geospiza Ancient DNA Bottleneck 

Notes

Acknowledgements

We thank Terry Chesser and Joel Cracraft of the American Museum of Natural History, and John Dumbacher, Maureen Flannery, Douglas Long and Luis Baptista of the California Academy of Science, and R. Prys-Jones of the British Natural History Museum for access to valuable historical specimens. We thank the Galápagos National Parks and Charles Darwin Research Station for field support. This work was partially supported by the National Science Foundation (DEB-0317687 to KP), Sigma Xi (HLF), The American Ornithologists’ Union (KP and HLF), and the University of Cincinnati University Research Council and Wieman-Wendell grant funds (HLF, KP, LPL).

Supplementary material

10592_2019_1175_MOESM1_ESM.xlsx (14 kb)
Supplementary material 1 Table 1 Museum specimen sources, accession numbers and collection dates. * = Specimen excluded from analysis due to <50% recovery of genotype data. CAS = California Academy of Science; ANHM = American Natural History Museum; BMNH = British Museum of Natural History (XLSX 14 KB)
10592_2019_1175_MOESM2_ESM.xlsx (12 kb)
Supplementary material 2 (XLSX 11 KB)
10592_2019_1175_MOESM3_ESM.docx (14 kb)
Supplementary material 3 (DOCX 13 KB)
10592_2019_1175_MOESM4_ESM.xlsx (14 kb)
Supplementary material 4 (XLSX 14 KB)
10592_2019_1175_MOESM5_ESM.pdf (288 kb)
Supplementary material 5 Fig. 1 PCA plot of microsatellite loci for historical and modern samples of Platyspiza crassirostris (excluded from Figure 2 due to the lack of modern data for the matched population). Individual populations are shown in different colors with color-matching 95% inertia ellipses designated for historical specimens. Microsatellite data and quantiNemo files are available from the authors on reasonable request (PDF 287 KB)

References

  1. Antao T, Pérez-Figueroa A, Luikart G (2011) Early detection of population declines: high power of genetic monitoring using effective population size estimators. Evol Appl 4:144–154.  https://doi.org/10.1111/j.1752-4571.2010.00150.x CrossRefGoogle Scholar
  2. Burkey TV (1995) Extinction rates in Archipelagoes: implications for populations in fragmented habitats. Conserv Biol 9:527–541.  https://doi.org/10.1046/j.1523-1739.1995.09030527.x CrossRefGoogle Scholar
  3. Caplins SA, Gilbert KJ, Ciotir C, Roland J, Matter SF, Keyghobadi N (2014) Landscape structure and the genetic effects of a population collapse. Proc R Soc Lond B 281:20141798.  https://doi.org/10.1098/rspb.2014.1798 CrossRefGoogle Scholar
  4. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  5. D’Elia J, McCarthy S (2010) Time horizons and extinction risk in endangered species categorization systems. Bioscience 60:751–758.  https://doi.org/10.1525/bio.2010.60.9.12 CrossRefGoogle Scholar
  6. Donlan CJ, Wilcox C (2008) Diversity, invasive species and extinctions in insular ecosystems. J Appl Ecol 45:1114–1123.  https://doi.org/10.1111/j.1365-2664.2008.01482.x CrossRefGoogle Scholar
  7. Drake JM (2014) Tail probabilities of extinction time in a large number of experimental populations. Ecology 95:1119–1126.  https://doi.org/10.1890/13-1107.1 CrossRefGoogle Scholar
  8. Dudaniec RY, Kleindorfer S (2006) Effects of the parasitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu 106:13–20.  https://doi.org/10.1071/MU04040 CrossRefGoogle Scholar
  9. Dvorak M, Fessl B, Nemeth E, Kleindorfer S, Tebbich S (2012) Distribution and abundance of Darwin’s finches and other land birds on Santa Cruz Island, Galápagos: evidence for declining populations. Oryx 46:78–86.  https://doi.org/10.1017/S0030605311000597 CrossRefGoogle Scholar
  10. Eckhardt RC (1972) Introduced plants and animals in the Galápagos Islands. Bioscience 22:585–590.  https://doi.org/10.2307/1296204 CrossRefGoogle Scholar
  11. Evans SR, Sheldon BC (2008) Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conserv Biol 22:1016–1025.  https://doi.org/10.1111/j.1523-1739.2008.00972.x CrossRefGoogle Scholar
  12. Fagan WF, Meir E, Prendergast J, Folarin A, Karieva P (2001) Characterizing population vulnerability for 758 species. Ecol Lett 4:132–138.  https://doi.org/10.1046/j.1461-0248.2001.00206.x CrossRefGoogle Scholar
  13. Farrington HL, Petren K (2011) A century of genetic change and metapopulation dynamics in the Galápagos Warbler Finches (certhidea). Evolution 65:3148–3161.  https://doi.org/10.1111/j.1558-5646.2011.01385.x CrossRefGoogle Scholar
  14. Farrington HL, Lawson LP, Clark CM, Petren K (2014) The evolutionary history of Darwin’s Finches: speciation, gene flow, and introgression in a fragmented landscape. Evolution 68:2932–2944.  https://doi.org/10.1111/evo.12484 CrossRefGoogle Scholar
  15. Frankham R, Ballou JD, Ralls K, Eldridge M, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, OxfordCrossRefGoogle Scholar
  16. Gaggiotti OE, Vetter RD (1999) Effect of life history strategy, environmental variability, and overexploitation on the genetic diversity of pelagic fish populations. Can J Fish Aquat Sci 56:1376–1388.  https://doi.org/10.1139/f99-060 Google Scholar
  17. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  18. Grant PR (1999) Ecology and evolution of Darwin’s finches. Princeton University Press, PrincetonGoogle Scholar
  19. Grant PR, Grant BR (1995) The founding of a new population of Darwin’s finches. Evolution 49:229–240.  https://doi.org/10.2307/2410333 CrossRefGoogle Scholar
  20. Grant PR, Grant BR (2009) The secondary contact phase of allopatric speciation in Darwin’s finches. PNAS 106:20141–20148.  https://doi.org/10.1073/pnas.0911761106 CrossRefGoogle Scholar
  21. Grant PR, Grant BR, Petren K, Keller LF (2005) Extinction behind our backs: the possible fate of one of the Darwin’s finch species on Isla Floreana, Galápagos. Biol Cons 122:499–503.  https://doi.org/10.1016/j.biocon.2004.09.001 CrossRefGoogle Scholar
  22. Hanski I, Gilpin M (1991) Metapopulation dynamics: brief history and conceptual domain. Biol J Linn Soc 42:3–16.  https://doi.org/10.1111/j.1095-8312.1991.tb00548.x CrossRefGoogle Scholar
  23. Hieb EE, Nelson DH, Morris AB (2014) Genetic monitoring reveals loss of microsatellite diversity in a breeding population of the endangered Alabama red-bellied turtle. Endang Species Res 23:253–261.  https://doi.org/10.3354/esr00581 CrossRefGoogle Scholar
  24. Johnson JA, Tingay RE, Culver M, Hailer F, Clarke ML, Mindell DP (2009) Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Mol Ecol 18:54–63.  https://doi.org/10.1111/j.1365-294X.2008.04012.x Google Scholar
  25. Keller LF, Jeffery KJ, Arcese P, Beaumont MA, Hochachka WM, Smith JNM, Bruford MW (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc R Soc Lond B 268:1387–1394.  https://doi.org/10.1098/rspb.2001.1607 CrossRefGoogle Scholar
  26. Kleindorfer S, Dudaniec RY (2016) Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zool 1:1.  https://doi.org/10.1186/s40850-016-0003-9 CrossRefGoogle Scholar
  27. Kleindorfer S, O’Connor JA, Dudaniec RY, Myers SA, Robertson J, Sulloway FJ (2014a) Species collapse via hybridization in Darwin’s Tree Finches. Am Nat 183:325–341.  https://doi.org/10.1086/674899 CrossRefGoogle Scholar
  28. Kleindorfer S, Peters KJ, Custance G, Dudaniec RY, O’Connor JA (2014b) Changes in Philornis infestation behavior threaten Darwin’s finch survival. Curr Zool 60:542–550CrossRefGoogle Scholar
  29. Lacy RC (1993) VORTEX: a computer simulation model for population viability analysis. Wildl Res 20:45–65.  https://doi.org/10.1071/wr9930045 CrossRefGoogle Scholar
  30. Lacy RC (2000) Structure of the VORTEX simulation model for population viability analysis. Ecol Bull 48:191–203Google Scholar
  31. Lamichhaney S, Berglund J, Almén MS, Maqbol K, Grabherr M, Martinez-Barrio A, Promerová M, Rubin C-J, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L (2015) Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371–375.  https://doi.org/10.1038/nature14181 CrossRefGoogle Scholar
  32. Lawson LP, Fessl B, Vargas FH, Farrington HL, Cunninghame HF, Mueller JC, Nemeth E, Sevilla PC, Petren K (2017) Slow motion extinction: inbreeding, outbreeding, and loss in the critically endangered mangrove finch (Camarhynchus heliobates). Conserv Genet 18:159–170.  https://doi.org/10.1007/s10592-016-0890-x) CrossRefGoogle Scholar
  33. Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic dataGoogle Scholar
  34. Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237.  https://doi.org/10.1111/j.1523-1739.1998.96388.x CrossRefGoogle Scholar
  35. Mace GM, Lande R (1991) Assessing extinction threats: toward a reevaluation of IUCN threatened species categories. Conserv Biol 5:148–157.  https://doi.org/10.1111/j.1523-1739.1991.tb00119.x CrossRefGoogle Scholar
  36. Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103.  https://doi.org/10.1038/nature06922 CrossRefGoogle Scholar
  37. Méndez M, Vögeli M, Tella JL, Godoy JA (2014) Joint effects of population size and isolation on genetic erosion in fragmented populations: finding fragmentation thresholds for management. Evol Appl 7:506–518.  https://doi.org/10.1111/eva.12154 CrossRefGoogle Scholar
  38. Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259.  https://doi.org/10.1111/j.1469-1809.1983.tb00993.x CrossRefGoogle Scholar
  39. Neuenschwander S, Hospital F, Guillaume F, Goudet J (2008) quantiNemo: an individual-based program to simulate quantitative traits with explicit genetic architecture in a dynamic metapopulation. Bioinformatics 24:1552–1553.  https://doi.org/10.1093/bioinformatics/btn219 CrossRefGoogle Scholar
  40. O’Connor JA, Dudaniec RY, Kleindorfer S (2010a) Parasite infestation and predation in Darwin’s small ground finch: contrasting two elevational habitats between islands. J Trop Ecol 26:285–292.  https://doi.org/10.1017/S0266467409990678 CrossRefGoogle Scholar
  41. O’Connor JA, Sulloway FJ, Kleindorfer S (2010b) Avian population survey in the Floreana highlands: is Darwin’s Medium Tree Finch declining in remnant patches of Scalesia forest? Bird Conserv Int 20:343–353.  https://doi.org/10.1017/S0959270910000195 CrossRefGoogle Scholar
  42. Parker PG, Buckles EL, Farrington H, Petren P, Whiteman NK, Ricklefs RE, Bollmer JL, Jiménez-Uzcátegui G (2011) 110 Years of avipoxvirus in the Galapagos Islands. PLoS ONE 6:e15989.  https://doi.org/10.1371/journal.pone.0015989 CrossRefGoogle Scholar
  43. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539.  https://doi.org/10.1093/bioinformatics/bts460 CrossRefGoogle Scholar
  44. Petren K, Grant BR, Grant PR (1999) A phylogeny of Darwin’s finches based on microsatellite DNA length variation. Proc R Soc Lond B 266:321–329.  https://doi.org/10.1098/rspb.1999.0641 CrossRefGoogle Scholar
  45. Petren K, Grant PR, Grant BR, Keller LF (2005) Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol Ecol 14:2943–2957.  https://doi.org/10.1111/j.1365-294X.2005.02632.x CrossRefGoogle Scholar
  46. Petren K, Grant PR, Grant BR, Clack AA, Lescano NV (2010) Multilocus genotypes from Charles Darwin’s finches: biodiversity lost since the voyage of the Beagle. Philos Trans R Soc Lond B 365:1009–1018.  https://doi.org/10.1098/rstb.2009.0316 CrossRefGoogle Scholar
  47. Pratt TK (2009) Conservation biology of Hawaiian forest birds: implications for Island Avifauna. Yale University Press, New HavenGoogle Scholar
  48. R Development Core Team (2018) R: A language and environment for statistical computingGoogle Scholar
  49. Reed DH (2010) Albatrosses, eagles and newts, Oh My!: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Anim Conserv 13:448–457.  https://doi.org/10.1111/j.1469-1795.2010.00353.x CrossRefGoogle Scholar
  50. Ridgway R (1896) Birds of the Galapagos Archipelago. U.S. Government Printing OfficeGoogle Scholar
  51. Rivera-Parra JL, Levin II, Parker PG (2014) Comparative Ectoparasite loads of five seabird species in the Galapagos Islands. J Parasitol 100:569–577.  https://doi.org/10.1645/12-141.1 CrossRefGoogle Scholar
  52. Sæther B-E, Engen S (2004) Stochastic population theory faces reality in the laboratory. Trends Ecol Evol 19:351–353.  https://doi.org/10.1016/j.tree.2004.05.003 CrossRefGoogle Scholar
  53. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33.  https://doi.org/10.1016/j.tree.2006.08.009 CrossRefGoogle Scholar
  54. Sefc KM, Payne RB, Sorenson MD, Fleischer RC (2003) Microsatellite amplification from museum feather samples: effects of fragment size and template concentration on genotyping errors. Auk 120:982–989CrossRefGoogle Scholar
  55. Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357.  https://doi.org/10.1111/j.1523-1739.2006.00524.x CrossRefGoogle Scholar
  56. Smyser TJ, Stauffer GE, Johnson SA, Hudson CM, Rhodes OE, Swihart RK (2016) Annual survival of Allegheny woodrats in a nonequilibrium metapopulation. J Mammal 97:1699–1708.  https://doi.org/10.1093/jmammal/gyw136 CrossRefGoogle Scholar
  57. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. PNAS 101:15261–15264.  https://doi.org/10.1073/pnas.0403809101 CrossRefGoogle Scholar
  58. Steadman DW (2006) Extinction and biogeography of tropical pacific birds. University of Chicago Press, ChicagoGoogle Scholar
  59. Steadman DW, Stafford TW Jr, Donahue DJ, Jull AJT (1991) Chronology of Holocene vertebrate extinction in the Galápagos Islands. Quat Res 36:126–133.  https://doi.org/10.1016/0033-5894(91)90021-V CrossRefGoogle Scholar
  60. Tonnis B, Grant PR, Grant BR, Petren K (2005) Habitat selection and ecological speciation in Galápagos warbler finches (Certhidea olivacea and Certhidea fusca). Proc R Soc Lond B 272:819–826.  https://doi.org/10.1098/rspb.2004.3030 CrossRefGoogle Scholar
  61. Trueman M, d’Ozouville N (2010) Characterizing the Galapagos terrestrial climate in the face of global climate change. Galapagos Res 67:26–37Google Scholar
  62. Watson J, Trueman M, Tufet M, Henderson S, Atkinson R (2010) Mapping terrestrial anthropogenic degradation on the inhabited islands of the Galápagos archipelago. Oryx 44:79–82.  https://doi.org/10.1017/S0030605309990226 CrossRefGoogle Scholar
  63. Wattier R, Engel CR, Saumitou-Laprade P, Valero M (1998) Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta). Mol Ecol 7:1569–1573.  https://doi.org/10.1046/j.1365-294x.1998.00477.x CrossRefGoogle Scholar
  64. Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  65. Wiggins IL, Porter DM (1971) Flora of the Galapagos Islands. Stanford University Press, StanfordGoogle Scholar
  66. Wikelski M, Foufopoulos J, Vargas H, Snell H (2004) Galápagos birds and diseases: invasive pathogens as threats for island species. Ecol Soc 9:5–15CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of CincinnatiCincinnatiUSA
  2. 2.Cincinnati Museum CenterCincinnatiUSA

Personalised recommendations