Predicting population extinctions in Darwin’s finches

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.

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Fig. 1
Fig. 2
Fig. 3

Source populations are shown in dark gray, while the sink population is shown in light gray—all with solid lines representing means and 95% confidence intervals. Dashed lines represent the mean from a non-metapopulation low-fitness population (K = 400 because K = 200 went extinct too rapidly for comparisons). a With source populations supplying immigrants to the sink population, population sizes of both source and sink populations were stable through time (solid lines). The size of the non-metapopulation low-fitness population (dashed) showed a decline in individuals. b Observed heterozygosity from 14 simulated microsatellite loci with 4 alleles each. In the metapopulation models, source and sink populations had indistinguishable means (black and dark gray solid lines). In the non-metapopulation low-fitness population (dashed line), the genetic diversity of the sink population declined rapidly. Results based on 10,000 simulations of 1000 generations with population size and genetic diversity recorded every 10 generations

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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).

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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)

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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)

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Farrington, H.L., Lawson, L.P. & Petren, K. Predicting population extinctions in Darwin’s finches. Conserv Genet 20, 825–836 (2019). https://doi.org/10.1007/s10592-019-01175-3

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Keywords

  • Extinction risk
  • Metapopulation dynamics
  • Geospiza
  • Ancient DNA
  • Bottleneck