Sex Chromosome-Linked Species Recognition and Evolution of Reproductive Isolation in Flycatchers

Stein A. Sæther,^1,2,3* Glenn-Peter Sætre,³ Thomas Borge,^2,3 Chris Wiley,^4,5 Nina Svedin,⁴ Gunilla Andersson,³ Thor Veen,⁶ Jon Haavie,^2,3 Maria R. Servedio,⁷ Stanislav Bure,⁸ Miroslav Král,⁹ Mårten B. Hjernquist,⁴ Lars Gustafsson,⁴ Johan Träff,¹⁰ Anna Qvarnström⁴

Interbreeding between species (hybridization) typically produces unfit offspring. Reduced hybridization should therefore be favored by natural selection. However, this is difficult to accomplish because hybridization also sets the stage for genetic recombination to dissociate species-specific traits from the preferences for them. Here we show that this association is maintained by physical linkage (on the same chromosome) in two hybridizing Ficedula flycatchers. By analyzing the mating patterns of female hybrids and cross-fostered offspring, we demonstrate that species recognition is inherited on the Z chromosome, which is also the known location of species-specific male plumage traits and genes causing low hybrid fitness. Limited recombination on the Z chromosome maintains associations of Z-linked genes despite hybridization, suggesting that the sex chromosomes may be a hotspot for adaptive speciation.

¹ Department of Animal Population Biology, Netherlands Institute of Ecology, Post Office Box 40, 6666 ZG Heteren, Netherlands.
² Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, Norbyvägen 18D, SE 75236 Uppsala, Sweden.
³ Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, Post Office Box 1050, Blindern, N 0316 Oslo, Norway.
⁴ Department of Animal Ecology, EBC, Uppsala University, Norbyvägen 18D, SE 75236 Uppsala, Sweden.
⁵ Department of Neurobiology and Behavior, Cornell University, Mudd Hall, Ithaca, NY 14853, USA.
⁶ Theoretical Biology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, Kerklaan 30, 9751 NN Haren, Netherlands.
⁷ Department of Biology, University of North Carolina, CB 3280 Coker Hall, Chapel Hill, NC 27599, USA.
⁸ Laboratory of Ornithology, Palack University, tida Svobody 26, 771 46 Olomouc, Czech Republic.
⁹ Forestry Commission, 783 86 Dlouhá Louka, Czech Republic.
¹⁰ Visborgsgatan 28 A, SE 621 58 Visby, Sweden.

^* To whom correspondence should be addressed. E-mail: s.a.sather{at}bio.uio.no

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