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McFarlane, S. E., Ålund, M., Sirkiä, P. M. & Qvarnström, A. (2018). Difference in plasticity of resting metabolic rate - the proximate explanation to different niche breadth in sympatric Ficedula flycatchers. Ecology and Evolution, 8(9), 4575-4586
Open this publication in new window or tab >>Difference in plasticity of resting metabolic rate - the proximate explanation to different niche breadth in sympatric Ficedula flycatchers
2018 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, no 9, p. 4575-4586Article in journal (Refereed) Published
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.

Keywords
cross-fostering, Ficedula flycatchers, plasticity, resting metabolic rate
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-356511 (URN)10.1002/ece3.3987 (DOI)000431987300020 ()29760898 (PubMedID)
Funder
Swedish Research Council, 621-2012-3722
Available from: 2018-08-10 Created: 2018-08-10 Last updated: 2018-08-10Bibliographically approved
Marzal, J. C., Rudh, A., Rogell, B., Ödeen, A., Lovlie, H., Rosher, C. & Qvarnström, A. (2017). Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner. Ecology and Evolution, 7(2), 744-750
Open this publication in new window or tab >>Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner
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2017 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 2, p. 744-750Article in journal (Refereed) Published
Abstract [en]

Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate-choosing females can favor corresponding changes in mate preferences. Our study system, Oophaga pumilio, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.

Keywords
aposematism, assortative mating, crypsis, Oophaga pumilio, predation, sexual selection, speciation
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-316051 (URN)10.1002/ece3.2662 (DOI)000392075300025 ()
Funder
Swedish Research Council
Available from: 2017-02-23 Created: 2017-02-23 Last updated: 2017-11-29Bibliographically approved
Segami Marzal, J. C., Rudh, A., Rogell, B., Ödeen, A., Lovlie, H., Rosher, C. & Qvarnström, A. (2017). Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner. Ecology and Evolution, 7(2), 744-750
Open this publication in new window or tab >>Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner
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2017 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 2, p. 744-750Article in journal (Refereed) Published
Abstract [en]

Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate-choosing females can favor corresponding changes in mate preferences. Our study system, Oophaga pumilio, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.

Keywords
aposematism, assortative mating, crypsis, Oophaga pumilio, predation, sexual selection, speciation
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-345094 (URN)
Funder
Swedish Research Council
Available from: 2018-03-07 Created: 2018-03-07 Last updated: 2018-03-07
Wheatcroft, D. & Qvarnström, A. (2017). Genetic divergence of early song discrimination between two young songbird species. NATURE ECOLOGY & EVOLUTION, 1(7), Article ID UNSP 0192.
Open this publication in new window or tab >>Genetic divergence of early song discrimination between two young songbird species
2017 (English)In: NATURE ECOLOGY & EVOLUTION, ISSN 2397-334X, Vol. 1, no 7, article id UNSP 0192Article in journal (Refereed) Published
Abstract [en]

Juvenile songbirds express species-specific song discrimination from an early age, which focuses learning onto the songs of their parental species. However, it remains unknown whether this early song discrimination is influenced by early social experience or maternal effects or whether it is instead largely genetically determined. We manipulated early social experience by swapping young embryos between the nests of two co-occurring songbird species-pied and collared flycatchers. We show that nestlings are more active in response to playbacks of conspecific songs, even when raised by adults from the other species, thus enabling us to reject social experience as the main determinant of early song discrimination. We then crossed the two species in captivity and showed that the song responses of hybrid nestlings do not depend on social experience or maternal species, implying genetic divergence of early song discrimination. Our results provide conclusive evidence that early song discrimination has a largely genetic component, which can stabilize reproductive isolation by reducing song learning across closely related species.

National Category
Genetics Zoology
Identifiers
urn:nbn:se:uu:diva-344538 (URN)10.1038/s41559-017-0192 (DOI)000417179000020 ()
Funder
Swedish Research CouncilThe Royal Swedish Academy of Sciences
Available from: 2018-03-07 Created: 2018-03-07 Last updated: 2018-03-07Bibliographically approved
Kardos, M., Qvarnström, A. & Ellegren, H. (2017). Inferring Individual Inbreeding and Demographic History from Segments of Identity by Descent in Ficedula Flycatcher Genome Sequences. Genetics, 205(3), 1319-1334
Open this publication in new window or tab >>Inferring Individual Inbreeding and Demographic History from Segments of Identity by Descent in Ficedula Flycatcher Genome Sequences
2017 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 205, no 3, p. 1319-1334Article in journal (Refereed) Published
Abstract [en]

Individual inbreeding and historical demography can be estimated by analyzing runs of homozygosity (ROH), which are indicative of chromosomal segments of identity by descent (IBD). Such analyses have so far been rare in natural populations due to limited genomic resources. We analyzed ROH in whole genome sequences from 287 Ficedula flycatchers representing four species, with the objectives of evaluating the causes of genome-wide variation in the abundance of ROH and inferring historical demography. ROH were clearly more abundant in genomic regions with low recombination rate. However, this pattern was substantially weaker when ROH were mapped using genetic rather than physical single nucleotide polymorphism (SNP) coordinates in the genome. Empirical results and simulations suggest that high ROH abundance in regions of low recombination was partly caused by increased power to detect the very long IBD segments typical of regions with a low recombination rate. Simulations also showed that hard selective sweeps (but not soft sweeps or background selection) likely contributed to variation in the abundance of ROH across the genome. Comparisons of the abundance of ROH among several study populations indicated that the Spanish pied flycatcher population had the smallest historical effective population size (Ne) for this species, and that a putatively recently founded island (Baltic) population had the smallest historical Ne among the collared flycatchers. Analysis of pairwise IBD in Baltic collared flycatchers indicated that this population was founded,60 generations ago. This study provides a rare genomic glimpse into demographic history and the mechanisms underlying the genome-wide distribution of ROH.

Place, publisher, year, edition, pages
GENETICS SOCIETY AMERICA, 2017
Keywords
runs of homozygosity, effective population size, population genomics
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-320356 (URN)10.1534/genetics.116.198861 (DOI)000395807200022 ()28100590 (PubMedID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg Foundation
Available from: 2017-04-19 Created: 2017-04-19 Last updated: 2018-02-22Bibliographically approved
Silva, C. N., McFarlane, S. E., Hagen, I. J., Ronnegard, L., Billing, A. M., Kvalnes, T., . . . Husby, A. (2017). Insights into the genetic architecture of morphological traits in two passerine bird species. Heredity, 119(3), 197-205
Open this publication in new window or tab >>Insights into the genetic architecture of morphological traits in two passerine bird species
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2017 (English)In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 119, no 3, p. 197-205Article in journal (Refereed) Published
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.

National Category
Evolutionary Biology Genetics and Breeding in Agricultural Sciences
Identifiers
urn:nbn:se:uu:diva-361050 (URN)10.1038/hdy.2017.29 (DOI)000407362100008 ()28613280 (PubMedID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationEU, European Research Council
Available from: 2018-09-20 Created: 2018-09-20 Last updated: 2018-09-20Bibliographically approved
Wheatcroft, D. & Qvarnström, A. (2017). Reproductive character displacement of female, but not male song discrimination in an avian hybrid zone. Evolution, 71(7), 1776-1786
Open this publication in new window or tab >>Reproductive character displacement of female, but not male song discrimination in an avian hybrid zone
2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 7, p. 1776-1786Article in journal (Refereed) Published
Abstract [en]

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co-occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of oland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on oland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co-occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
Ficedula, reinforcement, reproductive character displacement, sexual signals, song discrimination, species recognition
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-331248 (URN)10.1111/evo.13267 (DOI)000405888100004 ()28493350 (PubMedID)
Funder
Swedish Research CouncilThe Royal Swedish Academy of Sciences
Available from: 2017-10-24 Created: 2017-10-24 Last updated: 2017-10-24Bibliographically approved
Smeds, L., Mugal, C. F., Qvarnström, A. & Ellegren, H. (2016). High-Resolution Mapping of Crossover and Non-crossover Recombination Events by Whole-Genome Re-sequencing of an Avian Pedigree. PLoS Genetics, 12(5), Article ID e1006044.
Open this publication in new window or tab >>High-Resolution Mapping of Crossover and Non-crossover Recombination Events by Whole-Genome Re-sequencing of an Avian Pedigree
2016 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 12, no 5, article id e1006044Article in journal (Refereed) Published
Abstract [en]

Recombination is an engine of genetic diversity and therefore constitutes a key process in evolutionary biology and genetics. While the outcome of crossover recombination can readily be detected as shuffled alleles by following the inheritance of markers in pedigreed families, the more precise location of both crossover and non-crossover recombination events has been difficult to pinpoint. As a consequence, we lack a detailed portrait of the recombination landscape for most organisms and knowledge on how this landscape impacts on sequence evolution at a local scale. To localize recombination events with high resolution in an avian system, we performed whole-genome re-sequencing at high coverage of a complete three-generation collared flycatcher pedigree. We identified 325 crossovers at a median resolution of 1.4 kb, with 86% of the events localized to <10 kb intervals. Observed crossover rates were in excellent agreement with data from linkage mapping, were 52% higher in male (3.56 cM/Mb) than in female meiosis (2.28 cM/Mb), and increased towards chromosome ends in male but not female meiosis. Crossover events were non-randomly distributed in the genome with several distinct hot-spots and a concentration to genic regions, with the highest density in promoters and CpG islands. We further identified 267 non-crossovers, whose location was significantly associated with crossover locations. We detected a significant transmission bias (0.18) in favour of 'strong' (G, C) over 'weak' (A, T) alleles at non-crossover events, providing direct evidence for the process of GC-biased gene conversion in an avian system. The approach taken in this study should be applicable to any species and would thereby help to provide a more comprehensive portray of the recombination landscape across organism groups.

National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-296467 (URN)10.1371/journal.pgen.1006044 (DOI)000377197100044 ()27219623 (PubMedID)
Funder
Swedish Research Council, 2010-5650; 2013-8271EU, European Research Council, AdG 24997Knut and Alice Wallenberg Foundation
Available from: 2016-06-16 Created: 2016-06-16 Last updated: 2018-02-22Bibliographically approved
McFarlane, S. E., Sirkiä, P., Ålund, M. & Qvarnström, A. (2016). Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers. PLoS ONE, 11(9), Article ID e0161547.
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
Rönnegård, L., McFarlane, S. E., Husby, A., Kawakami, T., Ellegren, H. & Qvarnström, A. (2016). Increasing the power of genome wide association studies in natural populations using repeated measures - evaluation and implementation. Methods in Ecology and Evolution, 7(7), 792-799
Open this publication in new window or tab >>Increasing the power of genome wide association studies in natural populations using repeated measures - evaluation and implementation
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2016 (English)In: Methods in Ecology and Evolution, ISSN 2041-210X, E-ISSN 2041-210X, Vol. 7, no 7, p. 792-799Article in journal (Refereed) Published
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.

Keywords
Ficedula albicollis, genomic relationship, hierarchical generalized linear model, single-nucleotide polymorphisms
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-301427 (URN)10.1111/2041-210X.12535 (DOI)000379957400004 ()
Funder
EU, European Research CouncilKnut and Alice Wallenberg FoundationSwedish Research CouncilStiftelsen Olle Engkvist Byggmästare
Available from: 2016-08-23 Created: 2016-08-23 Last updated: 2018-08-10Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-1178-4053

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