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Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics. (Qvarnström)ORCID iD: 0000-0003-2861-9721
Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The complex nature of interspecific interactions contributing to reproductive isolation means that we still know little about their molecular basis. Male reproductive traits are notorious for their fast evolution at the phenotypic and genotypic level, and divergence in components of the ejaculate can lead to incompatibilities between closely related species. Making use of recent advances of molecular tools and the extensive knowledge on the biology and ecology of young sister species, here the pied (Ficedula hypoleuca) and collared flycatcher (F. albicollis), allows the identification of candidate phenotypes and the underlying genotypes maintaining species boundaries. Pied flycatcher females can avoid costly production of sterile hybrids when mated to collared flycatchers by cryptically favouring conspecific sperm. Here, we describe the testes transcriptome and sperm proteome of both species, confirm the complexity of avian sperm development and functions and identify several candidate genes for interactions between sperm and the female reproductive tract, using multiple independent measures of divergence between the species. We show that divergence at the transcriptional and translational levels can potentially lead to the evolution of reproductive incompatibilities despite low levels of sequence divergence, and suggest that integrating several -omics techniques with knowledge of the biology of naturally hybridizing species will greatly improve our understanding of the molecular basis of speciation in the near future. 

Keywords [en]
Reproductive isolation, cryptic female choice, sperm, proteomics, transcriptomics, Ficedula flycatchers
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-326809OAI: oai:DiVA.org:uu-326809DiVA, id: diva2:1128856
Available from: 2017-07-30 Created: 2017-07-30 Last updated: 2017-07-30
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. p. 67
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1533
Keywords
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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