Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks
1 Resource Ecology Group, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands
2 Conservation Genetics Group, Senckenberg Research Institute and Natural History Museum, D-63571 Gelnhausen, Germany
3 Department of Molecular Biology, Faculty of Science, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen, Nijmegen, The Netherlands
4 Animal Breeding and Genomics Centre, Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
5 Aquatic Biology and Chemistry, Kristianstad University, SE-291 88 Kristianstad, Sweden
6 Biological Station Rybachy of the Zoological institute RAS, 238535 Kaliningrad region, Russia
7 Ecological Watch of Siberia, Komarova street 27/6/5, 644074 Omsk, Russia
8 Department of Chemistry, Omsk State University, St. Prospect Mira 55a, 644077 Omsk, Russia
9 Centre for Wildlife Ecology, Simon Fraser University, V5A 1S6 Burnaby, BC, Canada
BMC Evolutionary Biology 2012, 12:45 doi:10.1186/1471-2148-12-45Published: 2 April 2012
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.
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.
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.