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Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Qvarnström)ORCID iD: 0000-0003-2861-9721
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 [en]
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: urn:nbn:se:uu:diva-326807ISBN: 978-91-513-0014-6 (print)OAI: oai:DiVA.org:uu-326807DiVA: diva2:1128857
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
List of papers
1. Sexual selection affects climate adaptation in collared flycatchers
Open this publication in new window or tab >>Sexual selection affects climate adaptation in collared flycatchers
2017 (English)Manuscript (preprint) (Other academic)
Abstract [en]

The role of sexual selection in climate adaptation is debated. We tested whether sexual selection has the potential to speed up adaptation to thermal conditions in a natural population of collared flycatchers. Based on a three-year cross-fostering experiment, we found that the size of a sexually selected trait predicted offspring metabolic rate: male collared flycatchers with large forehead patches sired offspring with low metabolic rate regardless of the ambient temperature. Thus, there was a stable significant relationship between forehead patch size of genetic fathers and offspring metabolic rate. Nestlings with high metabolic rate experienced a survival advantage when growing under warm temperatures, while the opposite was true in cold environments. Our study shows that females can modulate their offspring’s physiology through mate choice, and that sexual selection can thus affect climate adaptation.

Keyword
sexual selection, climate adaptation, resting metabolic rate, Ficedula flycatcher, secondary sexual character, physiology
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-322788 (URN)
Available from: 2017-07-30 Created: 2017-07-30 Last updated: 2017-07-30
2. Revisiting the definition of “sperm quality”: selection on sperm length depends on a male’s attractiveness and dominance in wild collared flycatchers
Open this publication in new window or tab >>Revisiting the definition of “sperm quality”: selection on sperm length depends on a male’s attractiveness and dominance in wild collared flycatchers
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Dominance over rivals, sexual attractiveness and highly efficient ejaculates are all known to be essential for male fertilization success but the theories of how primary and secondary sexual characters may co-evolve largely remain to be tested. Here, we measure sperm morphology in 131 wild-caught collared flycatchers over a four-year period and investigate the links between male display traits, sperm characteristics and siring success among 425 offspring sired by 71 of these males. We show that the optimal sperm length to attain high relative fertilization success depends on the size of a male’s secondary sexual character. Males with small ornaments sire more offspring in their own nest when they produce long sperm and vice-versa. These results are not compatible with theories based on simple relationships between secondary sexual traits and sperm “quality” but imply that the optimal fertilization strategy (and hence optimal sperm traits) differ between males even in a predominantly socially monogamous population with moderate extra-pair copulation rates. Thus, a better knowledge of the complex chain of behavioural interactions between the sexes and their gametes is needed for a complete understanding of how sexual selection operates in nature.

Keyword
sperm morphology, secondary sexual character, mating strategy, fertilization success, Ficedula flycatcher, extra-pair copulation
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-326808 (URN)
Available from: 2017-07-30 Created: 2017-07-30 Last updated: 2017-07-30
3. Low fertility of wild hybrid male flycatchers despite recent divergence
Open this publication in new window or tab >>Low fertility of wild hybrid male flycatchers despite recent divergence
2013 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, no 3, 20130169Article in journal (Refereed) Published
Abstract [en]

Postzygotic isolation may be important for maintaining species boundaries, particularly when premating barriers are incomplete. Little is known about the course of events leading from minor environmental mismatches affecting hybrid fitness to severe genetic incompatibilities causing sterility or inviability. We investigated whether reduced reproductive success of hybrid males was caused by suboptimal sperm traits or by more severe genetic incompatibilities in a hybrid zone of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) on the island of Oland, Sweden. About 4 per cent hybridization is observed in this population and all female hybrids are sterile. We found no sperm in the ejaculates of most sampled hybrid males, and sperm with abnormal morphology in two hybrids. Furthermore, none of the hybrids sired any offspring because of high levels of hatching failure and extra-pair paternity in their nests. These results from a natural hybrid zone suggest that the spermatogenesis of hybrid males may become disrupted despite little genetic divergence between the parental species.

Keyword
hybrid, sterility-infertility, flycatcher, sperm, postzygotic incompatibility
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-202341 (URN)10.1098/rsbl.2013.0169 (DOI)000318762300035 ()
Available from: 2013-06-24 Created: 2013-06-24 Last updated: 2017-12-06Bibliographically approved
4. Females discriminate against heterospecific sperm in a natural hybrid zone
Open this publication in new window or tab >>Females discriminate against heterospecific sperm in a natural hybrid zone
Show others...
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.

Keyword
Cryptic female choice, hybrid zones, postcopulatory prezygotic barriers, reinforcement, speciation, sexual selection
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-303102 (URN)10.1111/evo.12986 (DOI)000381205700013 ()
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
5. Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction
Open this publication in new window or tab >>Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction
Show others...
(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. 

Keyword
Reproductive isolation, cryptic female choice, sperm, proteomics, transcriptomics, Ficedula flycatchers
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-326809 (URN)
Available from: 2017-07-30 Created: 2017-07-30 Last updated: 2017-07-30

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