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Publications (10 of 15) Show all publications
Sirkiä, P. M., McFarlane, S. E., Jones, W., Wheatcroft, D., Ålund, M., Rybinski, J. & Qvarnström, A. (2018). Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.. Evolution, 72(2), 363-374
Open this publication in new window or tab >>Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.
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2018 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 2, p. 363-374Article in journal (Refereed) Published
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.

Keywords
Competitive exclusion, ecological speciation, prezygotic isolation, reinforcement, speciation, temporal segregation
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-341102 (URN)10.1111/evo.13404 (DOI)000424131100011 ()29214649 (PubMedID)
Funder
Swedish Research CouncilAcademy of Finland
Available from: 2018-02-06 Created: 2018-02-06 Last updated: 2019-03-10Bibliographically approved
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
Ålund, M., Persson Schmiterlöw, S., McFarlane, S. E. & Qvarnström, A. (2018). Optimal sperm length for high siring success depends on forehead patch size in collared flycatchers. Behavioral Ecology, 29(6), 1436-1443
Open this publication in new window or tab >>Optimal sperm length for high siring success depends on forehead patch size in collared flycatchers
2018 (English)In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 29, no 6, p. 1436-1443Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS INC, 2018
Keywords
extra-pair paternity, fertilization success, Ficedula flycatcher, mating strategy, secondary sexual character, sperm morphology
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-372829 (URN)10.1093/beheco/ary115 (DOI)000453209600033 ()
Funder
Swedish Research Council, VR 621-2012-3722
Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-01-09Bibliographically 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
McFarlane, S. E. (2017). Speciation and Metabolic rate: Insights from an avian hybrid zone. (Doctoral dissertation). Uppsala: Acta Universitatis Upsaliensis
Open this publication in new window or tab >>Speciation and Metabolic rate: Insights from an avian hybrid zone
2017 (English)Doctoral 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. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. p. 43
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1462
Keywords
resting metabolic rate, life history, hybridization, speciation, reproductive isolation, Ficedula flycatcher
National Category
Ecology Evolutionary Biology Genetics
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-309969 (URN)978-91-554-9776-7 (ISBN)
Public defence
2017-02-10, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-01-19 Created: 2016-12-08 Last updated: 2018-08-10
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
Kardos, M., Husby, A., McFarlane, S. E., Qvarnström, A. & Ellegren, H. (2016). Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations. Molecular Ecology Resources, 16(3), 727-741
Open this publication in new window or tab >>Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations
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2016 (English)In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 16, no 3, p. 727-741Article in journal (Refereed) Published
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.

Keywords
condition-dependent trait, fitness, genomewide association analysis, sexual selection
National Category
Biochemistry and Molecular Biology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-300299 (URN)10.1111/1755-0998.12498 (DOI)000373954100013 ()26649993 (PubMedID)
Funder
EU, European Research CouncilKnut and Alice Wallenberg FoundationSwedish Research CouncilStiftelsen Olle Engkvist Byggmästare
Available from: 2016-08-08 Created: 2016-08-08 Last updated: 2018-08-10Bibliographically approved
Qvarnström, A., Ålund, M., McFarlane, E. S. & Sirkiä, P. M. (2015). Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers. Evolutionary Applications, 9(1), 119-134
Open this publication in new window or tab >>Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers
2015 (English)In: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 9, no 1, p. 119-134Article, review/survey (Refereed) Published
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.

Keywords
ecological speciation;genetic incompatibilities;natural selection;personality;sexual selection;speciation genomics;thermal adaptation
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-261081 (URN)10.1111/eva.12276 (DOI)000368250500008 ()27087843 (PubMedID)
Funder
Swedish Research Council
Available from: 2015-08-28 Created: 2015-08-28 Last updated: 2018-08-10Bibliographically approved
McFarlane, S. E., Gorrell, J. C., Coltman, D. W., Humphries, M. M., Boutin, S. & McAdam, A. G. (2015). The nature of nurture in a wild mammal's fitness. Proceedings of the Royal Society of London. Biological Sciences, 282(1806), Article ID 20142422.
Open this publication in new window or tab >>The nature of nurture in a wild mammal's fitness
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2015 (English)In: 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) Published
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.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-252017 (URN)10.1098/rspb.2014.2422 (DOI)
Available from: 2015-04-28 Created: 2015-04-28 Last updated: 2018-08-10Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-0706-458x

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