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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
Ålund née Podevin, M. (2017). Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers. (Doctoral dissertation). Uppsala: Acta Universitatis Upsaliensis
Open this publication in new window or tab >>Sex, Sperm and Speciation: On sexual selection and fertility in hybridizing flycatchers
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Sexual reproduction entails complex co-evolution between the sexes, necessary for successful fertilization, ensuring individual and population-level fitness. Interfertility is the main criterion for species definition and understanding speciation requires detailed studies of reproductive barriers. However, many studies on reproductive barriers are constrained to infer evolutionary processes from patterns. In this thesis, I focus on a hybrid zone between collared and pied flycatchers (Ficedula albicollis and hypoleuca) on the island of Öland, and a trait that is essential for fertilization: sperm. Long-term monitoring of these species, combined with recent advances in molecular tools, allow me to study how complex on-going intersexual and interspecific interactions influence reproductive isolation in this young hybrid zone. I start by exploring the links between pre- and postmating sexual selection within collared flycatchers (paper I and II). I show that secondary sexual characters and indirect mate-choice benefits are tightly linked to physiology (paper I), and that a male’s attractiveness and dominance status dictate which sperm traits are optimal, as a male’s fertilization success depends on an interaction between sperm and display traits (paper II). I then report a source of strong postzygotic isolation between recently diverged collared and pied flycatchers: impaired spermatogenesis resulting in absence of mature sperm cells in hybrid males (paper III). I show however that pied flycatcher females, who are most exposed to hybridization, can mitigate these costs through mechanisms of cryptic female choice impairing heterospecific sperm performance, allowing them to bias paternity towards pure-species offspring (paper IV). Finally, by exploring the testes transcriptomes and sperm proteomes of both species, I highlight the importance of gene and protein regulation mechanisms in facilitating phenotypic divergence between these species (paper V). Thus, my thesis reveals complex interactions between primary and secondary sexual characters in a wild bird and suggests that mechanisms of sexual selection are tightly linked to essential physiological functions. I also show that genetic incompatibilities can evolve rapidly despite low genome-wide levels of divergence but that divergence in regulatory regions and proteins potentially allows fast evolution of molecular mechanisms impairing or preventing costly heterospecific fertilization. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. p. 67
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1533
Keywords
sperm biology, sexual selection, speciation, hybridization, cryptic female choice, fertility, Ficedula flycatchers
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-326807 (URN)978-91-513-0014-6 (ISBN)
Public defence
2017-09-15, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-08-23 Created: 2017-07-30 Last updated: 2017-09-08
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
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
Kawakami, T., Backström, N., Burri, R., Husby, A., Ólason, P., Rice, A. M., . . . Ellegren, H. (2014). Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array. Molecular Ecology Resources, 14(6), 1248-1260
Open this publication in new window or tab >>Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array
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2014 (English)In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 14, no 6, p. 1248-1260Article in journal (Refereed) Published
Abstract [en]

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

Keywords
collared flycatcher, GWAS, Hybridization, pied flycatcher, single-nucleotide polymorphism genotyping, speciation
National Category
Biochemistry and Molecular Biology Ecology
Identifiers
urn:nbn:se:uu:diva-237291 (URN)10.1111/1755-0998.12270 (DOI)000343805400014 ()24784959 (PubMedID)
Available from: 2014-12-03 Created: 2014-12-01 Last updated: 2018-02-22Bibliographically approved
Ålund, M., Immler, S., Rice, A. M. & Qvarnström, A. (2013). Low fertility of wild hybrid male flycatchers despite recent divergence. Biology Letters, 9(3), Article ID 20130169.
Open this publication in new window or tab >>Low fertility of wild hybrid male flycatchers despite recent divergence
2013 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, no 3, article id 20130169Article in journal (Refereed) Published
Abstract [en]

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

Keywords
hybrid, sterility-infertility, flycatcher, sperm, postzygotic incompatibility
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-202341 (URN)10.1098/rsbl.2013.0169 (DOI)000318762300035 ()
Available from: 2013-06-24 Created: 2013-06-24 Last updated: 2017-12-06Bibliographically approved
Ålund, M. (2012). Gametes and speciation: from prezygotic to postzygotic isolation (Introductoed.). Uppsala
Open this publication in new window or tab >>Gametes and speciation: from prezygotic to postzygotic isolation
2012 (English)Report (Other academic)
Abstract [en]

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

Place, publisher, year, edition, pages
Uppsala: , 2012. p. 33 Edition: Introducto
Series
Introductory Research Essay, ISSN 1404-4919 ; 100
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-261080 (URN)UU-ZEK-IRE–100–SE (ISRN)
Available from: 2015-08-28 Created: 2015-08-28 Last updated: 2015-09-07Bibliographically approved
Helfenstein, F., Podevin, M. & Richner, H. (2010). Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behavioral Ecology and Sociobiology, 64(4), 557-565
Open this publication in new window or tab >>Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus
2010 (English)In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 64, no 4, p. 557-565Article in journal (Refereed) Published
Abstract [en]

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

Keywords
passer domesticus, sperm competition, sperm flagellum, sperm length, sperm longevity, sperm midpiece, sperm morphology, sperm velocity
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-261079 (URN)10.1007/s00265-009-0871-x (DOI)
Available from: 2015-08-28 Created: 2015-08-28 Last updated: 2017-12-04Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0003-2861-9721

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