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  • 1. Helfenstein, Fabrice
    et al.
    Podevin, Murielle
    Universität Bern.
    Richner, Heinz
    Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus2010Ingår i: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 64, nr 4, s. 557-565Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Sperm competition exerts strong selection on males to produce spermatozoa with an optimal morphology that maximizes their fertilization success. Long sperm were first suggested to be favored because they should swim faster. However, studies that investigated the relationship between spermlength and sperm competitive ability or sperm swimming velocity yielded contradictory results. More recently, ratios of the different sections of a spermatozoon (the head,midpiece, and flagellum)were suggested to bemore crucial in determining swimming velocity. Additionally, sperm ability to remain and survive in the female storage organs may also influence fertilization success, so that optimal sperm morphology may rather maximize sperm longevity than velocity. In this study, we investigated how sperm morphology is related to sperm velocity and sperm longevity in the house sparrow Passer domesticus. Sperm velocity was found to be correlated with head/flagellum ratio. Sperm with small heads relative to their flagellum showed higher swimming velocity. Additionally, shorter sperm were found to live longer. Finally, we found sperm morphological traits to vary substantially within males and the head/flagellum ratio to be unrelated to total sperm length. We discuss the hypothesis that the substantial within-male variation in sperm morphology reflects a male strategy to produce a diversity of sperm from long, fast-swimming to short, long-living sperm to maximize their fertilization success in a context of sperm competition.

  • 2.
    Kawakami, Takeshi
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Backström, Niclas
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Burri, Reto
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Husby, Arild
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ólason, Páll
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Rice, Amber M.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array2014Ingår i: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 14, nr 6, s. 1248-1260Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    With the access to draft genome sequence assemblies and whole-genome resequencing data from population samples, molecular ecology studies will be able to take truly genome-wide approaches. This now applies to an avian model system in ecological and evolutionary research: Old World flycatchers of the genus Ficedula, for which we recently obtained a 1.1Gb collared flycatcher genome assembly and identified 13 million single-nucleotide polymorphism (SNP)s in population resequencing of this species and its sister species, pied flycatcher. Here, we developed a custom 50K Illumina iSelect flycatcher SNP array with markers covering 30 autosomes and the Z chromosome. Using a number of selection criteria for inclusion in the array, both genotyping success rate and polymorphism information content (mean marker heterozygosity=0.41) were high. We used the array to assess linkage disequilibrium (LD) and hybridization in flycatchers. Linkage disequilibrium declined quickly to the background level at an average distance of 17kb, but the extent of LD varied markedly within the genome and was more than 10-fold higher in genomic islands' of differentiation than in the rest of the genome. Genetic ancestry analysis identified 33 F-1 hybrids but no later-generation hybrids from sympatric populations of collared flycatchers and pied flycatchers, contradicting earlier reports of backcrosses identified from much fewer number of markers. With an estimated divergence time as recently as <1Ma, this suggests strong selection against F-1 hybrids and unusually rapid evolution of reproductive incompatibility in an avian system.

  • 3.
    McFarlane, S. Eryn
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sirkiä, Päivi
    Univ Helsinki, Finnish Museum Nat Hist, Zool Unit, Helsinki, Finland; Univ Turku, Sect Ecol, Dept Biol, Turku, Finland.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers2016Ingår i: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, nr 9, artikel-id e0161547Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Studies of ecological speciation are often biased towards extrinsic sources of selection against hybrids, resulting from intermediate hybrid morphology, but the knowledge of how genetic incompatibilities accumulate over time under natural conditions is limited. Here we focus on a physiological trait, metabolic rate, which is central to life history strategies and thermoregulation but is also likely to be sensitive to mismatched mitonuclear interactions. We measured the resting metabolic rate of male collared, and pied flycatchers as well as of naturally occurring F1 hybrid males, in a recent hybrid zone. We found that hybrid males had a higher rather than intermediate metabolic rate, which is indicative of hybrid physiological dysfunction. Fitness costs associated with elevated metabolic rate are typically environmentally dependent and exaggerated under harsh conditions. By focusing on male hybrid dysfunction in an eco-physiological trait, our results contribute to the general understanding of how combined extrinsic and intrinsic sources of hybrid dysfunction build up under natural conditions.

  • 4.
    McFarlane, S. Eryn
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. Univ Edinburgh, Inst Evolutionary Biol, Edinburgh, Midlothian, Scotland.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sirkiä, Paivi M.
    Univ Helsinki, Finnish Museum Nat Hist, Zool Unit, Helsinki, Finland; Univ Turku, Dept Biol, Sect Ecol, Turku, Finland.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Difference in plasticity of resting metabolic rate - the proximate explanation to different niche breadth in sympatric Ficedula flycatchers2018Ingår i: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, nr 9, s. 4575-4586Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Variation in relative fitness of competing recently formed species across heterogeneous environments promotes coexistence. However, the physiological traits mediating such variation in relative fitness have rarely been identified. Resting metabolic rate (RMR) is tightly associated with life history strategies, thermoregulation, diet use, and inhabited latitude and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have adapted to different climates in allopatry. We work in a long‐term study of collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) in a recent hybrid zone located on the Swedish island of Öland in the Baltic Sea. Here, we explore whether differences in RMR match changes in relative performance of growing flycatcher nestlings across environmental conditions using an experimental approach. The fitness of pied flycatchers has previously been shown to be less sensitive to the mismatch between the peak in food abundance and nestling growth among late breeders. Here, we find that pied flycatcher nestlings have lower RMR in response to higher ambient temperatures (associated with low food availability). We also find that experimentally relaxed nestling competition is associated with an increased RMR in this species. In contrast, collared flycatcher nestlings did not vary their RMR in response to these environmental factors. Our results suggest that a more flexible nestling RMR in pied flycatchers is responsible for the better adaptation of pied flycatchers to the typical seasonal changes in food availability experienced in this hybrid zone. Generally, subtle physiological differences that have evolved when species were in allopatry may play an important role to patterns of competition, coexistence, or displacements between closely related species in secondary contact.

  • 5.
    McFarlane, S. Eryn
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Sirkiä, Päivi M.
    Finnish Museum of Natural History, Zoology Unit, University of Helsinki, Finland.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Sexual selection affects climate adaptation in collared flycatchers2017Manuskript (preprint) (Övrigt vetenskapligt)
    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.

  • 6.
    McFarlane, S. Eryn
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. University of Helsinki.
    Sirkiä, Päivi
    University of Helsinki.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister speciesArtikel i tidskrift (Refereegranskat)
    Abstract [en]

    Differences in life history strategies of closely related species can result in variation in relative fitness across heterogeneous environments and promote coexistence. However, physiological mechanisms mediating such variation in relative fitness have not been identified. Resting metabolic rate (RMR) is tightly associated with life-history strategies and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have evolved to different climatic niches in allopatry. We explore whether differences in RMR match changes in relative fitness between collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) across environmental conditions experienced in a recent hybrid zone. We found a negative correlation between nestling RMR and temperatures experienced during growth in pied flycatchers, which was absent in collared flycatchers. This implies that pied flycatchers are better adapted to the typical seasonal changes in temperature and food availability experienced at these northern breeding sites. There was sufficient additive genetic variance in RMR to respond to selection in both species that may either facilitate ecological character displacement or lead to a breakdown of coexistence. Generally, subtle differences in climate adaptation may play an important role to patterns of competition, coexistence or displacements between closely related species at recent secondary contact.

  • 7.
    Qvarnström, Anna
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    McFarlane, Eryn S.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sirkiä, Päivi M.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers2015Ingår i: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 9, nr 1, s. 119-134Artikel, forskningsöversikt (Refereegranskat)
    Abstract [en]

    Climate adaptation is surprisingly rarely reported as a cause for the build-up of reproductive isolation between diverging populations. In this review, we summarize evidence for effects of climate adaptation on pre- and postzygotic isolation between emerging species with a particular focus on pied (Ficedula hypoleuca) and collared (Ficedula albicollis) flycatchers as a model for research on speciation. Effects of climate adaptation on prezygotic isolation or extrinsic selection against hybrids have been documented in several taxa, but the combined action of climate adaptation and sexual selection is particularly well explored in Ficedula flycatchers. There is a general lack of evidence for divergent climate adaptation causing intrinsic postzygotic isolation. However, we argue that the profound effects of divergence in climate adaptation on the whole biochemical machinery of organisms and hence many underlying genes should increase the likelihood of genetic incompatibilities arising as side effects. Fast temperature-dependent co-evolution between mitochondrial and nuclear genomes may be particularly likely to lead to hybrid sterility. Thus, how climate adaptation relates to reproductive isolation is best explored in relation to fast-evolving barriers to gene flow, while more research on later stages of divergence is needed to achieve a complete understanding of climate-driven speciation.

  • 8.
    Sirkiä, Päivi M
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    McFarlane, S. Eryn
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Jones, William
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Wheatcroft, David
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Rybinski, Jakub
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.2018Ingår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, nr 2, s. 363-374Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Divergence in the onset of reproduction can act as an important source of reproductive isolation (i.e., allochronic isolation) between co-occurring young species, but evidence for the evolutionary processes leading to such divergence is often indirect. While advancing spring seasons strongly affect the onset of reproduction in many taxa, it remains largely unexplored whether contemporary spring advancement directly affects allochronic isolation between young species. We examined how increasing spring temperatures affected onset of reproduction and thereby hybridization between pied and collared flycatchers (Ficedula spp.) across habitat types in a young secondary contact zone. We found that both species have advanced their timing of breeding in 14 years. However, selection on pied flycatchers to breed earlier was weaker, resulting in a slower response to advancing springs compared to collared flycatchers and thereby build-up of allochronic isolation between the species. We argue that a preadaptation to a broader niche use (diet) of pied flycatchers explains the slower response to raising spring temperature, but that reduced risk to hybridize may contribute to further divergence in the onset of breeding in the future. Our results show that minor differences in the response to environmental change of co-occurring closely related species can quickly cause allochronic isolation.

  • 9.
    Ålund, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Gametes and speciation: from prezygotic to postzygotic isolation2012Rapport (Övrigt vetenskapligt)
    Abstract [en]

    Speciation lies at the heart of evolutionary biology and researchers have been trying to understand the mechanisms leading to the evolution of reproductive isolation since over 250 years. Premating barriers (i.e. barriers preventing heterospecific individuals to mate with each other) and extrinsic postzygotic isolation (i.e. environmental factors affecting the fitness of hybrid individuals) have been studied in many taxa. However, little is known about what is happening at the gametic level, both before heterospecific fertilization (i.e. postmating prezygotic or gametic isolation) and in hybrid individuals (i.e. intrinsic postzygotic incompatibilities). In this essay, I will give an overview of the role gametes play in the evolution of reproductive isolation. I conclude that gametes and reproductive proteins evolve quickly, under strong influence of sexual and sexually antagonistic selection. Gametes are very diverse between species and sperm competition and female cryptic choice can lead to higher fertilization success of sperm from conspecific males. In the hybrid offspring, spermatogenesis can be easily disturbed by small differences in gene expression and this leads to a greater number of genes causing hybrid sterility compared to hybrid inviability among taxa. Following Haldane’s rule, the heterogametic sex is the first to be affected by hybrid incompatibilities, but different mechanisms seem to cause inviability and sterility and taxa with heterogametic males or heterogametic females might be affected differently. I end this review by focusing on one particular model system for studying speciation: the Ficedula flycatchers. Much is known about the ecological factors affecting speciation and hybridization between pied and collared flycatchers and new molecular data give insights into the genetics of speciation, but the role of gametes has not been studied in this system. Studies on gamete divergence and hybrid gamete production in the flycatchers will allow us to get a better idea of the role of gametes in speciation in a wild organism with homogametic males.

  • 10.
    Ålund, Murielle
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Immler, Simone
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Rice, Amber M.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Low fertility of wild hybrid male flycatchers despite recent divergence2013Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, nr 3, artikel-id 20130169Artikel i tidskrift (Refereegranskat)
    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.

  • 11.
    Ålund, Murielle
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. Michigan State Univ, Dept Integrat Biol, Giltner Hall 362, E Lansing, MI 48825 USA.
    Persson Schmiterlöw, Siri
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    McFarlane, S. Eryn
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. Univ Edinburgh, Inst Evolutionary Biol, Charlotte Auerbach Rd, Edinburgh EH9 3FL, Midlothian, Scotland.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Optimal sperm length for high siring success depends on forehead patch size in collared flycatchers2018Ingår i: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 29, nr 6, s. 1436-1443Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Dominance over rivals, sexual attractiveness, and highly efficient ejaculates are 3 important contributors of male fertilization success but theories about how primary and secondary sexual characters may co-evolve largely remain to be tested. We investigated how variation in a sexual signal (forehead patch size) and sperm morphology jointly affected siring success of 70 males in a natural population of collared flycatchers. We show that the optimal sperm length to attain high relative fertilization success depended on the size of a male's secondary sexual character. Males with small forehead patches sired more offspring in their nest when they produced long sperm and vice-versa. These results are not compatible with theories based on simple relationships between display traits and sperm "quality" but imply that the optimal fertilization strategy (and hence optimal sperm traits) differs between males even in a predominantly socially monogamous population with moderate extra-pair paternity 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.

  • 12.
    Ålund, Murielle
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Persson-Schmitterlöw, Siri
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    McFarlane, S. Eryn
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Revisiting the definition of “sperm quality”: selection on sperm length depends on a male’s attractiveness and dominance in wild collared flycatchersManuskript (preprint) (Övrigt vetenskapligt)
    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.

  • 13.
    Ålund, Murielle
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Whittington, Emma
    Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
    Backström, Niclas
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Borziak, Kirill
    Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
    Jones, Williams
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    McFarlane, S. Eryn
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Mugal, Carina F.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Wang, Mi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Wheatcroft, David
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Xu, Luohao
    University of Vienna, Austria.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Immler, Simone
    School of Biological Sciences, University of East Anglia, Norwich, Norfolk, NR4 7TJ, UK.
    Dorus, Steve
    Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interactionManuskript (preprint) (Övrigt vetenskapligt)
    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. 

  • 14.
    Ålund née Podevin, Murielle
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers2017Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
    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. 

    Delarbeten
    1. Sexual selection affects climate adaptation in collared flycatchers
    Öppna denna publikation i ny flik eller fönster >>Sexual selection affects climate adaptation in collared flycatchers
    2017 (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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.

    Nyckelord
    sexual selection, climate adaptation, resting metabolic rate, Ficedula flycatcher, secondary sexual character, physiology
    Nationell ämneskategori
    Evolutionsbiologi
    Identifikatorer
    urn:nbn:se:uu:diva-322788 (URN)
    Tillgänglig från: 2017-07-30 Skapad: 2017-07-30 Senast uppdaterad: 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
    Öppna denna publikation i ny flik eller fönster >>Revisiting the definition of “sperm quality”: selection on sperm length depends on a male’s attractiveness and dominance in wild collared flycatchers
    (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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.

    Nyckelord
    sperm morphology, secondary sexual character, mating strategy, fertilization success, Ficedula flycatcher, extra-pair copulation
    Nationell ämneskategori
    Evolutionsbiologi
    Identifikatorer
    urn:nbn:se:uu:diva-326808 (URN)
    Tillgänglig från: 2017-07-30 Skapad: 2017-07-30 Senast uppdaterad: 2017-07-30
    3. Low fertility of wild hybrid male flycatchers despite recent divergence
    Öppna denna publikation i ny flik eller fönster >>Low fertility of wild hybrid male flycatchers despite recent divergence
    2013 (Engelska)Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, nr 3, artikel-id 20130169Artikel i tidskrift (Refereegranskat) 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.

    Nyckelord
    hybrid, sterility-infertility, flycatcher, sperm, postzygotic incompatibility
    Nationell ämneskategori
    Biologiska vetenskaper
    Identifikatorer
    urn:nbn:se:uu:diva-202341 (URN)10.1098/rsbl.2013.0169 (DOI)000318762300035 ()
    Tillgänglig från: 2013-06-24 Skapad: 2013-06-24 Senast uppdaterad: 2017-12-06Bibliografiskt granskad
    4. Females discriminate against heterospecific sperm in a natural hybrid zone
    Öppna denna publikation i ny flik eller fönster >>Females discriminate against heterospecific sperm in a natural hybrid zone
    Visa övriga...
    2016 (Engelska)Ingår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, nr 8, s. 1844-1855Artikel i tidskrift (Refereegranskat) 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.

    Nyckelord
    Cryptic female choice, hybrid zones, postcopulatory prezygotic barriers, reinforcement, speciation, sexual selection
    Nationell ämneskategori
    Evolutionsbiologi
    Identifikatorer
    urn:nbn:se:uu:diva-303102 (URN)10.1111/evo.12986 (DOI)000381205700013 ()
    Forskningsfinansiär
    Vetenskapsrådet, 621-2012-3722Kungliga Vetenskapsakademien
    Tillgänglig från: 2016-10-05 Skapad: 2016-09-15 Senast uppdaterad: 2018-08-10Bibliografiskt granskad
    5. Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction
    Öppna denna publikation i ny flik eller fönster >>Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interaction
    Visa övriga...
    (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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. 

    Nyckelord
    Reproductive isolation, cryptic female choice, sperm, proteomics, transcriptomics, Ficedula flycatchers
    Nationell ämneskategori
    Evolutionsbiologi
    Identifikatorer
    urn:nbn:se:uu:diva-326809 (URN)
    Tillgänglig från: 2017-07-30 Skapad: 2017-07-30 Senast uppdaterad: 2017-07-30
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