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  • 1.
    Cramer, Emily R. A.
    et al.
    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..
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Johnsen, Arild
    Univ Oslo, Nat Hist Museum, N-0318 Oslo, Norway..
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Females discriminate against heterospecific sperm in a natural hybrid zone2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 8, p. 1844-1855Article in journal (Refereed)
    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.

  • 2.
    Jones, William
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Mozūraitis, Raimondas
    Institute of Zoology, Stockholm University.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Emami, S. Noushin
    Department of Molecular Biosciences, Wenner-Gren Institute, Stockholm University.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Malaria infected birds produce higher levels of vector-attracting compoundsManuscript (preprint) (Other academic)
  • 3.
    Kardos, Marty
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Husby, Arild
    Univ Helsinki, Dept Biosci, POB 65, FIN-00014 Helsinki, Finland.;Norwegian Univ Sci & Technol, Ctr Biodivers Dynam, Dept Biol, N-7491 Trondheim, Norway..
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations2016In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 16, no 3, p. 727-741Article in journal (Refereed)
    Abstract [en]

    Dissecting the genetic basis of phenotypic variation in natural populations is a long-standing goal in evolutionary biology. One open question is whether quantitative traits are determined only by large numbers of genes with small effects, or whether variation also exists in large-effect loci. We conducted genomewide association analyses of forehead patch size (a sexually selected trait) on 81 whole-genome-resequenced male collared flycatchers with extreme phenotypes, and on 415 males sampled independent of patch size and genotyped with a 50K SNP chip. No SNPs were genomewide statistically significantly associated with patch size. Simulation-based power analyses suggest that the power to detect large-effect loci responsible for 10% of phenotypic variance was <0.5 in the genome resequencing analysis, and <0.1 in the SNP chip analysis. Reducing the recombination by two-thirds relative to collared flycatchers modestly increased power. Tripling sample size increased power to >0.8 for resequencing of extreme phenotypes (N=243), but power remained <0.2 for the 50K SNP chip analysis (N=1245). At least 1 million SNPs were necessary to achieve power >0.8 when analysing 415 randomly sampled phenotypes. However, power of the 50K SNP chip to detect large-effect loci was nearly 0.8 in simulations with a small effective population size of 1500. These results suggest that reliably detecting large-effect trait loci in large natural populations will often require thousands of individuals and near complete sampling of the genome. Encouragingly, far fewer individuals and loci will often be sufficient to reliably detect large-effect loci in small populations with widespread strong linkage disequilibrium.

  • 4.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Speciation and Metabolic rate: Insights from an avian hybrid zone2017Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The role of divergent climate adaptation in speciation has received surprisingly little scientific attention. My dissertation research focused on how resting metabolic rate (RMR) relates to the build up of prezygotic and postzygotic isolation in a natural Ficedula flycatcher hybrid zone. RMR is the amount of energy an organism needs to run its internal organs. Since RMR is related to life history traits and thermoregulation in other systems, it is likely to affect speciation processes at secondary contact. I found that adult collared flycatchers displace pied flycatchers into increasingly poor habitats (Paper I). Pied nestlings exhibit lower RMR in poor environments (Paper II), which may promote regional coexistence and habitat isolation by making it possible for pied flycatchers to escape competition from collared flycatchers and reduce the risk of hybridization by breeding in the poorer habitats. Further, I found that while collared flycatcher nestling RMR was not environmentally-dependent (Paper II, Paper III), those collared flycatcher nestlings that had a lower RMR in poor environments tended to have higher condition (Paper III). Further, RMR was genetically linked to a sexual ornament in collared males that has previously been shown to be beneficial in poor environments. Lastly, I found that by seven days old, nestlings increase their metabolic rate when listening to song, indicating that they are listening, and by 9 days they can discriminate between songs (Paper IV). Taken together, RMR could affect pre-zygotic isolation via correlations with life history strategies, song and sexual ornaments. RMR is also related to post zygotic isolation in Ficedula flycatchers. I found that flycatcher hybrids tended to have a higher RMR than the parental species (Paper V), and that there were many differentially expressed genes in energetically expensive organs in hybrids that were related to metabolic function (Paper VI). Thus, metabolic dysfunction, possibly caused by genetic incompatibilities, in Ficedula flycatcher hybrids could be a factor leading to infertility and postzygotic isolation between the parental species. Overall, I find that RMR could be a general physiological trait that affects both pre- and postzygotic isolation in hybridizing species at secondary contact, and ought to be more thoroughly considered in speciation research. 

    List of papers
    1. Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone
    Open this publication in new window or tab >>Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone
    Show others...
    2016 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 10, p. 2226-2238Article in journal (Refereed) Published
    Abstract [en]

    Competition-driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on-going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition-driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future "voluntarily" altered immigration patterns and possibly strengthened habitat isolation through reinforcement.

    Keywords
    Competitive exclusion, ecological speciation, habitat segregation, prezygotic isolation, speciation
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-307727 (URN)10.1111/evo.13019 (DOI)000385550700005 ()27464950 (PubMedID)
    Funder
    Swedish Research Council
    Available from: 2016-11-21 Created: 2016-11-21 Last updated: 2018-08-10Bibliographically approved
    2. Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister species
    Open this publication in new window or tab >>Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister species
    (English)Article in journal (Refereed) Submitted
    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.

    National Category
    Natural Sciences Ecology
    Identifiers
    urn:nbn:se:uu:diva-309966 (URN)
    Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2018-08-10Bibliographically approved
    3. Sexual selection affects climate adaptation in collared flycatchers
    Open this publication in new window or tab >>Sexual selection affects climate adaptation in collared flycatchers
    (English)Article in journal (Refereed) Submitted
    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 new thermal environments 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 low metabolic rate experienced a survival advantage when growing under high temperatures, which is consistent with the prediction that a low metabolic rate confers a fitness advantage in warm climates. Our study shows that sexual selection can affect climate adaptation. 

    Keywords
    sexual selection, climate adaptation, resting metabolic rate, Ficedula flycatcher
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-309967 (URN)
    Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2018-08-10
    4. Song discrimination by nestling collared flycatchers during early development
    Open this publication in new window or tab >>Song discrimination by nestling collared flycatchers during early development
    2016 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 12, no 7, article id 20160234Article in journal (Refereed) Published
    Abstract [en]

    Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatty with closely related species.

    Keywords
    species recognition, song, metabolic rate, Ficedula flycatcher
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-303751 (URN)10.1098/rsbl.2016.0234 (DOI)000382423700005 ()
    Funder
    Swedish Research Council
    Available from: 2016-09-23 Created: 2016-09-23 Last updated: 2018-08-10Bibliographically approved
    5. Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers
    Open this publication in new window or tab >>Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers
    2016 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 9, article id e0161547Article in journal (Refereed) Published
    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.

    National Category
    Zoology
    Identifiers
    urn:nbn:se:uu:diva-307010 (URN)10.1371/journal.pone.0161547 (DOI)000382855600038 ()
    Funder
    Swedish Research Council, 621-2012-3722
    Available from: 2016-12-08 Created: 2016-11-08 Last updated: 2018-08-10Bibliographically approved
    6. RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair
    Open this publication in new window or tab >>RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair
    Show others...
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Hybrid dysfunction is thought to gradually build up through the accumulation of clashes between genes as they diverge between the parental species. However, analyses of genetic incompatibilities are generally biased towards long diverged species that are kept under laboratory conditions. Here, we used RNAseq to evaluate 1) whether there was differential gene expression between naturally occurring Ficedula flycatcher hybrids and parental species in energetically expensive alimentary organs, and 2) if such differential gene expression was, based on Gene Ontology (GO) terms, functionally related to Resting Metabolic Rate (RMR) and energy production. We found substantial differential gene expression in all pairwise contrasts, but fewer functional differences between the parental species than between hybrids and either parental species. Some of the differentially expressed genes underlay the OXPHOS pathway, and significantly more than expected GO terms associated with metabolic function were differentially expressed between hybrids and either parental species in the liver. Our results corroborate the idea that tightly co-evolved mitochondrial and nuclear genes underlying the Oxidative Phosphorylation (OXPHOS) pathway can become miss-matched in hybrids and cause malfunctioning phenotypes. Mitonuclear interactions affecting OXPHOS have the potential to both quickly diverge in allopatry as populations adapt to different climate regimes and to cause hybrid genetic dysfunction at secondary contact 

    Keywords
    Dobzhansky Muller interactions, RNA seq, mitonuclear incompatibility, genetic incompatibility, Resting metabolic rate, hybrid, Ficedula flycatcher
    National Category
    Evolutionary Biology Genetics
    Identifiers
    urn:nbn:se:uu:diva-309968 (URN)
    Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2018-08-10
  • 5.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Gorrell, Jamieson C.
    Coltman, David W.
    Humphries, Murray M.
    Boutin, Stan
    McAdam, Andrew G.
    The nature of nurture in a wild mammal's fitness2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, no 1806, article id 20142422Article in journal (Refereed)
    Abstract [en]

    Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population's adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population's evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.

  • 6. McFarlane, S. Eryn
    et al.
    Gorrell, Jamieson C.
    Coltman, David W.
    Humphries, Murray M.
    Boutin, Stan
    McAdam, Andrew G.
    Very low levels of direct additive genetic variance in fitness and fitness components in a red squirrel population2014In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 4, no 10, p. 1729-1738Article in journal (Refereed)
    Abstract [en]

    A trait must genetically correlate with fitness in order to evolve in response to natural selection, but theory suggests that strong directional selection should erode additive genetic variance in fitness and limit future evolutionary potential. Balancing selection has been proposed as a mechanism that could maintain genetic variance if fitness components trade off with one another and has been invoked to account for empirical observations of higher levels of additive genetic variance in fitness components than would be expected from mutation-selection balance. Here, we used a long-term study of an individually marked population of North American red squirrels (Tamiasciurus hudsonicus) to look for evidence of (1) additive genetic variance in lifetime reproductive success and (2) fitness trade-offs between fitness components, such as male and female fitness or fitness in high- and low-resource environments. Animal model analyses of a multigenerational pedigree revealed modest maternal effects on fitness, but very low levels of additive genetic variance in lifetime reproductive success overall as well as fitness measures within each sex and environment. It therefore appears that there are very low levels of direct genetic variance in fitness and fitness components in red squirrels to facilitate contemporary adaptation in this population.

  • 7.
    McFarlane, S. Eryn
    et al.
    Department of Integrative Biology, University of Guelph.
    Lane, Jeffrey E.
    Taylor, Ryan W.
    Gorrell, Jamieson C.
    Coltman, David W.
    Humphries, Murray M.
    Boutin, Stan
    McAdam, Andrew G.
    The heritability of multiple male mating in a promiscuous mammal2011In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 7, no 3, p. 368-371Article in journal (Refereed)
    Abstract [en]

    The tendency of females to mate with multiple males is often explained by direct and indirect benefits that could outweigh the many potential costs of multiple mating. However, behaviour can only evolve in response to costs and benefits if there is sufficient genetic variation on which selection can act. We followed 108 mating chases of 85 North American red squirrels (Tamiasciurus hudsonicus) during 4 years, to measure each female's degree of multiple male mating (MMM), and used an animal model analysis of our multi-generational pedigree to provide what we believe is the first estimate of the heritability of MMM in the wild. Female red squirrels were highly polyandrous, mating with an average of 7.0 ± 0.2 males on their day of oestrus. Although we found evidence for moderate levels of additive genetic variation (CVA = 5.1), environmental variation was very high (CVE = 32.3), which resulted in a very low heritability estimate (h2 < 0.01). So, while there is genetic variation in this trait, the large environmental variation suggests that any costs or benefits associated with differences among females in MMM are primarily owing to environmental and not genetic differences, which could constrain the evolutionary response to natural selection on this trait.

  • 8.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Päivi
    Univ Helsinki, Finnish Museum Nat Hist, Zool Unit, Helsinki, Finland; Univ Turku, Sect Ecol, Dept Biol, Turku, Finland.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers2016In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 9, article id e0161547Article in journal (Refereed)
    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.

  • 9.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Söderberg, Axel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Wheatcroft, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Song discrimination by nestling collared flycatchers during early development2016In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 12, no 7, article id 20160234Article in journal (Refereed)
    Abstract [en]

    Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatty with closely related species.

  • 10.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Wheatcroft, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Jones, William
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Xu, Luohao
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    van der Valk, Tom
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pairManuscript (preprint) (Other academic)
    Abstract [en]

    Hybrid dysfunction is thought to gradually build up through the accumulation of clashes between genes as they diverge between the parental species. However, analyses of genetic incompatibilities are generally biased towards long diverged species that are kept under laboratory conditions. Here, we used RNAseq to evaluate 1) whether there was differential gene expression between naturally occurring Ficedula flycatcher hybrids and parental species in energetically expensive alimentary organs, and 2) if such differential gene expression was, based on Gene Ontology (GO) terms, functionally related to Resting Metabolic Rate (RMR) and energy production. We found substantial differential gene expression in all pairwise contrasts, but fewer functional differences between the parental species than between hybrids and either parental species. Some of the differentially expressed genes underlay the OXPHOS pathway, and significantly more than expected GO terms associated with metabolic function were differentially expressed between hybrids and either parental species in the liver. Our results corroborate the idea that tightly co-evolved mitochondrial and nuclear genes underlying the Oxidative Phosphorylation (OXPHOS) pathway can become miss-matched in hybrids and cause malfunctioning phenotypes. Mitonuclear interactions affecting OXPHOS have the potential to both quickly diverge in allopatry as populations adapt to different climate regimes and to cause hybrid genetic dysfunction at secondary contact 

  • 11.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Edinburgh, Inst Evolutionary Biol, Edinburgh, Midlothian, Scotland.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Paivi M.
    Univ Helsinki, Finnish Museum Nat Hist, Zool Unit, Helsinki, Finland; Univ Turku, Dept Biol, Sect Ecol, Turku, Finland.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Difference in plasticity of resting metabolic rate - the proximate explanation to different niche breadth in sympatric Ficedula flycatchers2018In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, no 9, p. 4575-4586Article in journal (Refereed)
    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.

  • 12.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Sirkiä, Päivi M.
    Finnish Museum of Natural History, Zoology Unit, University of Helsinki, Finland.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Sexual selection affects climate adaptation in collared flycatchers2017Manuscript (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.

  • 13.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. University of Helsinki.
    Sirkiä, Päivi
    University of Helsinki.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister speciesArticle in journal (Refereed)
    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.

  • 14.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Päivi
    University of Helsinki.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sexual selection affects climate adaptation in collared flycatchersArticle in journal (Refereed)
    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 new thermal environments 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 low metabolic rate experienced a survival advantage when growing under high temperatures, which is consistent with the prediction that a low metabolic rate confers a fitness advantage in warm climates. Our study shows that sexual selection can affect climate adaptation. 

  • 15. Noble, Daniel W. A.
    et al.
    McFarlane, Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Keogh, J. Scott
    Whiting, Martin J.
    Maternal and additive genetic effects contribute to variation in offspring traits in a lizard2014In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 25, no 3Article in journal (Refereed)
    Abstract [en]

    Evolutionary responses to selection require that traits have a heritable basis, yet maternal effects (the effect of a mother's phenotype on her offspring's phenotype) can have profound effects on evolutionary processes. It is therefore essential to understand how maternal effects contribute to phenotypic variation in offspring traits and test key assumptions of additive genetic variance in evolutionary models. We measured 5 traits linked to fitness in lizards (endurance, sprint speed, snout-vent length [SVL], mass, and growth rate) and estimated the contribution of additive genetic and maternal effects in explaining variation in these traits in the Eastern water skink (Eulamprus quoyii). We estimated parentage using 6 microsatellite DNA loci from lizards taking part in a mating experiment in large seminatural enclosures and used animal models to partition variance into additive genetic and maternal effects. We found that only endurance was significantly heritable (h(2) = 0.37, 95% credible interval = 0.18-0.50), whereas all other traits were either strongly influenced by maternal effects (mass, sprint speed, SVL, and captive growth rate) or were influenced by environmental variability (wild growth rate). Our study disentangles the relative contributions of additive genetic and maternal effects in contributing to variation in offspring phenotypes and suggests that little additive genetic variance exists for traits often assumed to be heritable. Although the heritability of phenotypic traits is essential in evolutionary models, our results also highlight the important role maternal effects have in explaining variation in phenotypes.

  • 16.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    McFarlane, Eryn S.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Päivi M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers2015In: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 9, no 1, p. 119-134Article, review/survey (Refereed)
    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.

  • 17.
    Rybinski, Jakub
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkia, Paivi M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Helsinki, Zool Unit, Finnish Museum Nat Hist, FIN-00014 Helsinki, Finland..
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Vallin, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Wheatcroft, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 10, p. 2226-2238Article in journal (Refereed)
    Abstract [en]

    Competition-driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on-going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition-driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future "voluntarily" altered immigration patterns and possibly strengthened habitat isolation through reinforcement.

  • 18.
    Rönnegård, Lars
    et al.
    Swedish Univ Agr Sci, Dept Clin Sci, SE-75007 Uppsala, Sweden..
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Husby, Arild
    Univ Helsinki, Metapopulat Res Ctr, Dept Biosci, POB 65, FI-00014 Helsinki, Finland.;Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, N-7491 Trondheim, Norway..
    Kawakami, Takeshi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Increasing the power of genome wide association studies in natural populations using repeated measures - evaluation and implementation2016In: Methods in Ecology and Evolution, ISSN 2041-210X, E-ISSN 2041-210X, Vol. 7, no 7, p. 792-799Article in journal (Refereed)
    Abstract [en]

    1. Genomewide association studies (GWAS) enable detailed dissections of the genetic basis for organisms' ability to adapt to a changing environment. In long-term studies of natural populations, individuals are often marked at one point in their life and then repeatedly recaptured. It is therefore essential that a method for GWAS includes the process of repeated sampling. In a GWAS, the effects of thousands of single-nucleotide polymorphisms (SNPs) need to be fitted and any model development is constrained by the computational requirements. A method is therefore required that can fit a highly hierarchical model and at the same time is computationally fast enough to be useful. 2. Our method fits fixed SNP effects in a linear mixed model that can include both random polygenic effects and permanent environmental effects. In this way, the model can correct for population structure and model repeated measures. The covariance structure of the linear mixed model is first estimated and subsequently used in a generalized least squares setting to fit the SNP effects. The method was evaluated in a simulation study based on observed genotypes from a long-term study of collared flycatchers in Sweden. 3. The method we present here was successful in estimating permanent environmental effects from simulated repeated measures data. Additionally, we found that especially for variable phenotypes having large variation between years, the repeated measurements model has a substantial increase in power compared to a model using average phenotypes as a response. 4. The method is available in the R package RepeatABEL. It increases the power in GWAS having repeated measures, especially for long-term studies of natural populations, and the R implementation is expected to facilitate modelling of longitudinal data for studies of both animal and human populations.

  • 19.
    Silva, C. N. S.
    et al.
    Univ Helsinki, Dept Biosci, Metapopulat Res Ctr, Helsinki, Finland;James Cook Univ, Coll Marine & Environm Sci, Ctr Sustainable Trop Fisheries & Aquaculture, Townsville, Qld, Australia.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hagen, I. J.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Ronnegard, L.
    Swedish Univ Agr Sci, Dept Anim Breeding & Genet, Uppsala, Sweden;Dalarna Univ, Sch Technol & Business Studies, Falun, Sweden.
    Billing, A. M.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Kvalnes, T.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Kemppainen, P.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Ronning, B.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Ringsby, T. H.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Saether, B-E
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Jensen, H.
    Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Husby, A.
    Univ Helsinki, Dept Biosci, Metapopulat Res Ctr, Helsinki, Finland;Norwegian Univ Sci & Technol, Dept Biol, Ctr Biodivers Dynam, Trondheim, Norway.
    Insights into the genetic architecture of morphological traits in two passerine bird species2017In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 119, no 3, p. 197-205Article in journal (Refereed)
    Abstract [en]

    Knowledge about the underlying genetic architecture of phenotypic traits is needed to understand and predict evolutionary dynamics. The number of causal loci, magnitude of the effects and location in the genome are, however, still largely unknown. Here, we use genome-wide single-nucleotide polymorphism (SNP) data from two large-scale data sets on house sparrows and collared flycatchers to examine the genetic architecture of different morphological traits (tarsus length, wing length, body mass, bill depth, bill length, total and visible badge size and white wing patches). Genomic heritabilities were estimated using relatedness calculated from SNPs. The proportion of variance captured by the SNPs (SNP-based heritability) was lower in house sparrows compared with collared flycatchers, as expected given marker density (6348 SNPs in house sparrows versus 38 689 SNPs in collared flycatchers). Indeed, after downsampling to similar SNP density and sample size, this estimate was no longer markedly different between species. Chromosome-partitioning analyses demonstrated that the proportion of variance explained by each chromosome was significantly positively related to the chromosome size for some traits and, generally, that larger chromosomes tended to explain proportionally more variation than smaller chromosomes. Finally, we found two genome-wide significant associations with very small-effect sizes. One SNP on chromosome 20 was associated with bill length in house sparrows and explained 1.2% of phenotypic variation (V-P), and one SNP on chromosome 4 was associated with tarsus length in collared flycatchers (3% of V-P). Although we cannot exclude the possibility of undetected large-effect loci, our results indicate a polygenic basis for morphological traits.

  • 20.
    Sirkiä, Päivi M
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Jones, William
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Wheatcroft, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rybinski, Jakub
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.2018In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 2, p. 363-374Article in journal (Refereed)
    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.

  • 21.
    Ålund, Murielle
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Michigan State Univ, Dept Integrat Biol, Giltner Hall 362, E Lansing, MI 48825 USA.
    Persson Schmiterlöw, Siri
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Edinburgh, Inst Evolutionary Biol, Charlotte Auerbach Rd, Edinburgh EH9 3FL, Midlothian, Scotland.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Optimal sperm length for high siring success depends on forehead patch size in collared flycatchers2018In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 29, no 6, p. 1436-1443Article in journal (Refereed)
    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.

  • 22.
    Ålund, Murielle
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Persson-Schmitterlöw, Siri
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Revisiting the definition of “sperm quality”: selection on sperm length depends on a male’s attractiveness and dominance in wild collared flycatchersManuscript (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.

  • 23.
    Ålund, Murielle
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Whittington, Emma
    Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Borziak, Kirill
    Center for Reproductive Evolution, 248 Life Sciences Complex, Syracuse, NY 13244, USA.
    Jones, Williams
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Mugal, Carina F.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Wang, Mi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Wheatcroft, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Xu, Luohao
    University of Vienna, Austria.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    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 University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Reproductive -omics of a wild avian speciation model unveils candidate genes for gamete interactionManuscript (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. 

1 - 23 of 23
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