TY - JOUR
T1 - Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks
AU - Kraus, Robert H.S.
AU - Kerstens, Hindrik H.D.
AU - Van Hooft, Pim
AU - Megens, Hendrik Jan
AU - Elmberg, Johan
AU - Tsvey, Arseny
AU - Sartakov, Dmitry
AU - Soloviev, Sergej A.
AU - Crooijmans, Richard P.M.A.
AU - Groenen, Martien A.M.
AU - Ydenberg, Ronald C.
AU - Prins, Herbert H.T.
N1 - Funding Information:
We are thankful to the following persons and institutions for providing Anas platyrhynchos samples: Ernst Niedermayer, Hans Jörg Damm (Stiftung Fürst Liechtenstein, Austria), David Rodrigues (Escola Superior Agrária de Coimbra, Portugal), Brandt Meixell, Danielle Mondloch, Jonathan Runstadler (University of Alaska Fairbanks, USA), V.N. Stepanov, O. Tutenkov, V.I. Zalogin, Sergey Gashkov, Sergey Fokin (State Informational-Analytical Centre of Game Animal and Environment of Hunting Department of Russia), Urmas Võro, David Lamble, Garry Grigg, Aaron Everingham, Holly Middleton (Simon Fraser University, Vancouver, Canada). Rolik Grzegorz (Zoo Opole, Poland), Magnus Hellström (Ottenby Bird Observatory, Sweden), Michael Wink, Javier Gonzales (University of Heidelberg, Germany), Dirk Ullrich (Alpenzoo Innsbruck, Austria), Kamil Čihák (Zoo Dvur Kralove, Czech Republic), Marina Euler (Tierpark Lange Erlen, Switzerland), Sascha Knauf (Opel Zoo, Germany), Yang Liu (University of Bern, Switzerland), Mathieu Boos (CNRS Strasbourg, France), Crystal Matthews (Virginia Aquarium, USA), Timm Spretke (Zoologischer Garten Halle, Germany) and Valery Buzun provided samples from duck species other than Anas platyrhynchos. Technical assistance with genotyping was provided by Bert Dibbits. Daniël Goedbloed helped with the software package Eigenstrat. We thank Michael Turelli and Carlo Dietl for discussions. Javier Gonzales provided unpublished data on divergence times of duck species, and Brian Cade helped with statistics. The WWT, Slimbridge, UK, provided drawings for Figure 1. This work was financially supported by the KNJV (Royal Netherlands Hunters Association), the Dutch Ministry of Agriculture, the Faunafonds and the Stichting de Eik trusts (both in The Netherlands) and the Swedish Environmental Protection Agency, grants V-220-08 and V-205-09.
PY - 2012
Y1 - 2012
N2 - Background: The study of speciation and maintenance of species barriers is at the core of evolutionary biology. During speciation the genome of one population becomes separated from other populations of the same species, which may lead to genomic incompatibility with time. This separation is complete when no fertile offspring is produced from inter-population matings, which is the basis of the biological species concept. Birds, in particular ducks, are recognised as a challenging and illustrative group of higher vertebrates for speciation studies. There are many sympatric and ecologically similar duck species, among which fertile hybrids occur relatively frequently in nature, yet these species remain distinct. Results: We show that the degree of shared single nucleotide polymorphisms (SNPs) between five species of dabbling ducks (genus Anas) is an order of magnitude higher than that previously reported between any pair of eukaryotic species with comparable evolutionary distances. We demonstrate that hybridisation has led to sustained exchange of genetic material between duck species on an evolutionary time scale without disintegrating species boundaries. Even though behavioural, genetic and ecological factors uphold species boundaries in ducks, we detect opposing forces allowing for viable interspecific hybrids, with long-term evolutionary implications. Based on the superspecies concept we here introduce the novel term "supra- population" to explain the persistence of SNPs identical by descent within the studied ducks despite their history as distinct species dating back millions of years. Conclusions: By reviewing evidence from speciation theory, palaeogeography and palaeontology we propose a fundamentally new model of speciation to accommodate our genetic findings in dabbling ducks. This model, we argue, may also shed light on longstanding unresolved general speciation and hybridisation patterns in higher organisms, e.g. in other bird groups with unusually high hybridisation rates. Observed parallels to horizontal gene transfer in bacteria facilitate the understanding of why ducks have been such an evolutionarily successful group of animals. There is large evolutionary potential in the ability to exchange genes among species and the resulting dramatic increase of effective population size to counter selective constraints.
AB - Background: The study of speciation and maintenance of species barriers is at the core of evolutionary biology. During speciation the genome of one population becomes separated from other populations of the same species, which may lead to genomic incompatibility with time. This separation is complete when no fertile offspring is produced from inter-population matings, which is the basis of the biological species concept. Birds, in particular ducks, are recognised as a challenging and illustrative group of higher vertebrates for speciation studies. There are many sympatric and ecologically similar duck species, among which fertile hybrids occur relatively frequently in nature, yet these species remain distinct. Results: We show that the degree of shared single nucleotide polymorphisms (SNPs) between five species of dabbling ducks (genus Anas) is an order of magnitude higher than that previously reported between any pair of eukaryotic species with comparable evolutionary distances. We demonstrate that hybridisation has led to sustained exchange of genetic material between duck species on an evolutionary time scale without disintegrating species boundaries. Even though behavioural, genetic and ecological factors uphold species boundaries in ducks, we detect opposing forces allowing for viable interspecific hybrids, with long-term evolutionary implications. Based on the superspecies concept we here introduce the novel term "supra- population" to explain the persistence of SNPs identical by descent within the studied ducks despite their history as distinct species dating back millions of years. Conclusions: By reviewing evidence from speciation theory, palaeogeography and palaeontology we propose a fundamentally new model of speciation to accommodate our genetic findings in dabbling ducks. This model, we argue, may also shed light on longstanding unresolved general speciation and hybridisation patterns in higher organisms, e.g. in other bird groups with unusually high hybridisation rates. Observed parallels to horizontal gene transfer in bacteria facilitate the understanding of why ducks have been such an evolutionarily successful group of animals. There is large evolutionary potential in the ability to exchange genes among species and the resulting dramatic increase of effective population size to counter selective constraints.
UR - http://www.scopus.com/inward/record.url?scp=84859126568&partnerID=8YFLogxK
U2 - 10.1186/1471-2148-12-45
DO - 10.1186/1471-2148-12-45
M3 - Article
C2 - 22462721
AN - SCOPUS:84859126568
SN - 1471-2148
VL - 12
JO - BMC Evolutionary Biology
JF - BMC Evolutionary Biology
IS - 1
M1 - 45
ER -