Multilocus genotypes from Charles Darwin's finches: biodiversity lost since the voyage of the Beagle
Abstract
Genetic analysis of museum specimens offers a direct window into a past that can predate the loss of extinct forms. We genotyped 18 Galápagos finches collected by Charles Darwin and companions during the voyage of the Beagle in 1835, and 22 specimens collected in 1901. Our goals were to determine if significant genetic diversity has been lost since the Beagle voyage and to determine the genetic source of specimens for which the collection locale was not recorded. Using ‘ancient’ DNA techniques, we quantified variation at 14 autosomal microsatellite loci. Assignment tests showed several museum specimens genetically matched recently field-sampled birds from their island of origin. Some were misclassified or were difficult to classify. Darwin's exceptionally large ground finches (Geospiza magnirostris) from Floreana and San Cristóbal were genetically distinct from several other currently existing populations. Sharp-beaked ground finches (Geospiza difficilis) from Floreana and Isabela were also genetically distinct. These four populations are currently extinct, yet they were more genetically distinct from congeners than many other species of Darwin's finches are from each other. We conclude that a significant amount of the finch biodiversity observed and collected by Darwin has been lost since the voyage of the Beagle.
Footnotes
References
-
Allendorf F. W.& Luikart G. . 2007 Conservation and the genetics of populations. Malden, MA: Blackwell. Google Scholar -
Arandjelovic M., Guschanski K., Schubert G., Harris T. R., Thalmann O., Siedel H.& Vigilant L. . 2009 Two-step multiplex PCR improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol. Ecol. Resour. 9, 28–36. (doi:10.1111/j.1755-0998.2008.02387.x). Crossref, PubMed, ISI, Google Scholar -
Bonin A., Bellemain E., Bronken E. P., Pompanon F., Brochmann C.& Taberlet P. . 2004 How to track and assess genotyping errors in population genetics studies. Mol. Ecol. 13, 3261–3273. (doi:10.1111/j.1365-294X.2004.02346.x). Crossref, PubMed, ISI, Google Scholar -
Darwin C. R. . 1859 On the origin of species by means of natural selection. London, UK: John Murray. Google Scholar -
Dvorak M., Vargas H., Fessl B.& Tebbich S. . 2004 On the verge of extinction: a survey of the mangrove finch Cactospiza heliobates and its habitat on the Galápagos Islands. Oryx 38, 171–179. (doi:10.1017/S0030605304000316). Crossref, ISI, Google Scholar -
Ellegren H. . 2004 Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5, 435–445. (doi:10.1038/nrg1348). Crossref, PubMed, ISI, Google Scholar -
Fessl B., Kleindorfer S.& Tebbich S. . 2006 An experimental study on the effects of an introduced parasite in Darwin's finches. Biol. Conserv. 127, 55–61. (doi:10.1016/j.biocon.2005.07.013). Crossref, ISI, Google Scholar -
Gilbert M. T. P., Bandelt H.-J., Hofreiter M.& Barnes I. . 2005 Assessing ancient DNA studies. Trends Ecol. Evol. 20, 541–544. (doi:10.1016/j.tree.2005.07.005). Crossref, PubMed, ISI, Google Scholar -
Grant P. R. . 1999 Ecology and evolution in Darwin's finches. Princeton, NJ: Princeton University Press. Google Scholar -
Grant K. T.& Estes G. B. . 2009 Darwin in Galápagos: footsteps to a New World. Princeton, NJ: Princeton University Press. Google Scholar -
Grant P. R.& Grant B. R. . 1997a The rarest of Darwin's finches. Conserv. Biol. 11, 119–126. (doi:10.1046/j.1523-1739.1997.95399.x). Crossref, ISI, Google Scholar -
Grant P. R.& Grant B. R. . 1997b Mating patterns of Darwin's finch hybrids determined by song and morphology. Biol. J. Linn. Soc. 60, 317–343. (doi:10.1111/j.1095-8312.1997.tb01499.x). Crossref, ISI, Google Scholar -
Grant P. R.& Grant B. R. . 2002 Unpredictable evolution in a 30-year study of Darwin's finches. Science 296, 707–711. (doi:10.1126/science.1070315). Crossref, PubMed, ISI, Google Scholar -
Grant P. R.& Grant B. R. . 2006 Evolution of character displacement in Darwin's finches. Science 313, 224–226. (doi:10.1126/science.1128374). Crossref, PubMed, ISI, Google Scholar -
Grant P. R.& Grant B. R. . 2009 The secondary contact phase of allopatric speciation in Darwin's finches. Proc. Natl Acad. Sci. USA 106, 20 141–20 148 (advanced online) (doi:10.1073/pnas.0911761106). Crossref, ISI, Google Scholar -
Grant P. R., Grant B. R.& Petren K. . 2000 The allopatric phase of speciation: the sharp-beaked ground finch (Geospiza difficilis) on the Galápagos Islands. Biol. J. Linn. Soc. 69, 287–317. (doi:10.1111/j.1095-8312.2000.tb01207.x). Crossref, ISI, Google Scholar -
Grant P. R., Grant B. R., Keller L. F., Markert J. A.& Petren K. . 2003 Inbreeding and interbreeding in Darwin's finches. Evolution 57, 2911–2916. Crossref, PubMed, ISI, Google Scholar -
Grant P. R., Grant B. R., Markert J. A., Keller L. F.& Petren K. . 2004 Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution 58, 1588–1599. Crossref, PubMed, ISI, Google Scholar -
Grant P. R., Grant B. R., Petren K.& Keller L. F. . 2005a Extinction behind our backs: the possible fate of one of the Darwin's finch species on Isla Floreana, Galápagos. Biol. Conserv. 122, 499–503. (doi:10.1016/j.biocon.2004.09.001). Crossref, ISI, Google Scholar -
Grant P. R., Grant B. R.& Petren K. . 2005b Hybridization in the recent past. Am. Nat. 166, 56–67. (doi:10.1086/430331). Crossref, PubMed, ISI, Google Scholar -
Groombridge J. J., Jones C. G., Bruford M. W.& Nichols R. A. . 2000 ‘Ghost’ alleles of the Mauritius kestrel. Nature 403, 616. (doi:10.1038/35001148). Crossref, PubMed, ISI, Google Scholar -
Hedrick P.& Waits L. . 2005 What ancient DNA tells us. Heredity 94, 463–464. (doi:10.1038/sj.hdy.6800647). Crossref, PubMed, ISI, Google Scholar -
Herrmann B.& Hummel S. . 1994 Ancient DNA: recovery and analysis of genetic material from paleontological, archaeological, museum, medical and forensic specimens. New York, NY: Springer. Crossref, Google Scholar -
Lundh J. P. . 2001 Galápagos: a brief history. ISBN 82-92294-00-7. See http://www.lundh.no/jacob/Galapagos. Google Scholar -
Mundy N. I.& Woodruff D. S. . 1997 Skin from feet of museum specimens as a non-destructive source of DNA for avian genotyping. Auk 114, 126–129. Crossref, ISI, Google Scholar -
Nei M. . 1972 Genetic distance between populations. Am. Nat. 106, 283–292. (doi:10.1086/282771). Crossref, ISI, Google Scholar -
Paetkau D., Slade R., Burdens M.& Estoup A. . 2004 Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation based exploration of accuracy and power. Mol. Ecol. 13, 55–65. (doi:10.1046/j.1365-294X.2004.02008.x). Crossref, PubMed, ISI, Google Scholar -
Peakall R.& Smouse P. E. . 2006 Population genetic software for teaching and research (Genalex 6.0). Mol. Ecol. Notes 6, 288–295. (doi:10.1111/j.1471-8286.2005.01155.x). Crossref, Google Scholar -
Petren K. . 1998 Microsatellite primers from Geospiza fortis and cross-species amplification in Darwin's finches. Mol. Ecol. 7, 1782–1784. Crossref, PubMed, ISI, Google Scholar -
Petren K., Grant B. R.& Grant P. R. . 1999a A phylogeny of Darwin's finches based on microsatellite DNA length variation. Proc. R Soc. Lond. B 266, 321–329. (doi:10.1098/rspb.1999.0641). Link, ISI, Google Scholar -
Petren K., Grant B. R.& Grant P. R. . 1999b Low extrapair paternity in the cactus finch (Geospiza scandens). Auk 116, 252–256. Crossref, ISI, Google Scholar -
Petren K., Grant P. R., Grant B. R.& Keller L. F. . 2005 Comparative landscape genetics and the adaptive radiation of Darwin's finches: the role of peripheral isolation. Mol. Ecol. 14, 2943–2957. (doi:10.1111/j.1365-294X.2005.02632.x). Crossref, PubMed, ISI, Google Scholar -
Petren K., Farrington H., Fessl B., Vargas H.& Clack A. A. In preparation. A genetic signature of impending extinction in Darwin's rarest finch. Google Scholar -
Piry S., Alapetite A., Cornuet J., Paetkau D., Baudouin L.& Estoup A. . 2004 Geneclass2: a software for genetic assignment and first generation migrant detection. J. Hered. 95, 536–539. (doi:10.1093/jhered/esh074). Crossref, PubMed, ISI, Google Scholar -
Pritchard J. K., Stephens M.& Donnelly P. . 2000 Inference of population structure using multilocus genotype data. Genetics 155, 945–959. Crossref, PubMed, ISI, Google Scholar -
Schluter D.& Grant P. R. . 1982 The distribution of G. difficilis in relation to G. fuliginosa in the Galápagos Islands: tests of three hypotheses. Evolution 36, 1213–1226. (doi:10.2307/2408154). PubMed, ISI, Google Scholar -
Schluter D., Ratcliffe L. M.& Grant P. R. . 1991 The taxonomic status of the small Genovesa ground-finch in the Galápagos. Auk 108, 201–204. ISI, Google Scholar -
Steadman D. . 1986 Holocene vertebrate fossils from Isla Floreana, Galápagos. Smithsonian Contrib. Zool. 413, 1–104. Crossref, Google Scholar -
Sulloway F. J. . 1982 The Beagle collections of Darwin's finches [Geospizinae]. Bull. Br. Mus. [Nat. Hist.] Zool. Ser. 43, 49. Google Scholar -
Sulloway F. J. . 1983a Darwin and his finches: the evolution of a legend. J. Hist. Biol. 15, 1–53. (doi:10.1007/BF00132004). Crossref, Google Scholar -
Sulloway F. J. . 1983b The legend of Darwin's finches. Nature 303, 372. (doi:10.1038/303372a0). Crossref, ISI, Google Scholar -
Swarth H. S. . 1931 The avifauna of the Galápagos Islands. Occ. Pap. Cal. Acad. Sci. 18, 1–299. Google Scholar -
Taberlet P., Griffin S., Goossens B., Questiau S., Manceau V., Escaravage N., Waits L. P.& Bouvet J. . 1996 Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res. 24, 3189–3194. (doi:10.1093/nar/24.16.3189). Crossref, PubMed, ISI, Google Scholar -
Thiel T., Whiteman N. K., Tirape A., Maquero M. I., Cedeno V., Walsh T., Jimenez G.& Parker P. G. . 2005 Characterization of Canarypox-like viruses infecting endemic birds in the Galápagos Islands. J. Wildl. Dis. 41, 342–353. Crossref, PubMed, ISI, Google Scholar -
Tonnis B., Grant P. R., Grant B. R.& Petren K. . 2005 Habitat selection and ecological speciation in Galápagos warbler finches (Certhidea olivacea and Certhidea fusca). Proc. R. Soc. B 272, 819–826. (doi:10.1098/rspb.2004.3030). Link, ISI, Google Scholar -
Wandeler P., Hoeck P. A. E.& Keller L. F. . 2007 Back to the future: museum specimens in population genetics. Trends Ecol. Evol. 22, 634–642. (doi:10.1016/j.tree.2007.08.017). Crossref, PubMed, ISI, Google Scholar -
Watkins G.& Cruz F. . 2007 Galápagos at risk: a socioeconomic analysis of the situation in the archipelago. Puerto Ayora, Ecuador: Charles Darwin Foundation. Google Scholar -
Westemeier R. L., Brawn J. D., Simpson S. A., Esker T. L., Jansen R. W., Walk J. W., Kershner E. L., Bouzat J. L.& Paige K. N. . 1998 Tracking the long-term decline and recovery of an isolated population. Science 282, 1695–1698. (doi:10.1126/science.282.5394.1695). Crossref, PubMed, ISI, Google Scholar -
Wikelski M., Foufopoulos J., Vargas H.& Snell H. . 2004 Galápagos birds and diseases: invasive pathogens as threats for island species. Ecol. Soc. 9, 5. (http://www.ecologyandsociety.org/vol9/iss1/art5). Crossref, ISI, Google Scholar