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Females discriminate against heterospecific sperm in a natural hybrid zone
Univ Oslo, Nat Hist Museum, N-0318 Oslo, Norway.;Smithsonian Migratory Bird Ctr, POB 37012 MRC5503, Washington, DC 20008 USA.;Cornell Lab Ornithol, Ithaca, NY 14850 USA..
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
Univ Oslo, Nat Hist Museum, N-0318 Oslo, Norway..
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2016 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 8, 1844-1855 p.Article in journal (Refereed) Published
Abstract [en]

When hybridization is maladaptive, species-specific mate preferences are selectively favored, but low mate availability may constrain species-assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long-term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement-like process.

Place, publisher, year, edition, pages
2016. Vol. 70, no 8, 1844-1855 p.
Keyword [en]
Cryptic female choice, hybrid zones, postcopulatory prezygotic barriers, reinforcement, speciation, sexual selection
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-303102DOI: 10.1111/evo.12986ISI: 000381205700013OAI: oai:DiVA.org:uu-303102DiVA: diva2:1032985
Funder
Swedish Research Council, 621-2012-3722The Royal Swedish Academy of Sciences
Available from: 2016-10-05 Created: 2016-09-15 Last updated: 2017-11-30Bibliographically approved
In thesis
1. Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers
Open this publication in new window or tab >>Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Sexual reproduction entails complex co-evolution between the sexes, necessary for successful fertilization, ensuring individual and population-level fitness. Interfertility is the main criterion for species definition and understanding speciation requires detailed studies of reproductive barriers. However, many studies on reproductive barriers are constrained to infer evolutionary processes from patterns. In this thesis, I focus on a hybrid zone between collared and pied flycatchers (Ficedula albicollis and hypoleuca) on the island of Öland, and a trait that is essential for fertilization: sperm. Long-term monitoring of these species, combined with recent advances in molecular tools, allow me to study how complex on-going intersexual and interspecific interactions influence reproductive isolation in this young hybrid zone. I start by exploring the links between pre- and postmating sexual selection within collared flycatchers (paper I and II). I show that secondary sexual characters and indirect mate-choice benefits are tightly linked to physiology (paper I), and that a male’s attractiveness and dominance status dictate which sperm traits are optimal, as a male’s fertilization success depends on an interaction between sperm and display traits (paper II). I then report a source of strong postzygotic isolation between recently diverged collared and pied flycatchers: impaired spermatogenesis resulting in absence of mature sperm cells in hybrid males (paper III). I show however that pied flycatcher females, who are most exposed to hybridization, can mitigate these costs through mechanisms of cryptic female choice impairing heterospecific sperm performance, allowing them to bias paternity towards pure-species offspring (paper IV). Finally, by exploring the testes transcriptomes and sperm proteomes of both species, I highlight the importance of gene and protein regulation mechanisms in facilitating phenotypic divergence between these species (paper V). Thus, my thesis reveals complex interactions between primary and secondary sexual characters in a wild bird and suggests that mechanisms of sexual selection are tightly linked to essential physiological functions. I also show that genetic incompatibilities can evolve rapidly despite low genome-wide levels of divergence but that divergence in regulatory regions and proteins potentially allows fast evolution of molecular mechanisms impairing or preventing costly heterospecific fertilization. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. 67 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1533
Keyword
sperm biology, sexual selection, speciation, hybridization, cryptic female choice, fertility, Ficedula flycatchers
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-326807 (URN)978-91-513-0014-6 (ISBN)
Public defence
2017-09-15, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-08-23 Created: 2017-07-30 Last updated: 2017-09-08

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