| 1. |
- Chase, Madeline, et al.
(author)
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The combination of HiFi and HiC sequencing technologies enables the investigation of structural variants in speciation of Ficedula flycatchers
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Other publication (other academic/artistic)abstract
- Structural variants, typically defined as mutations affecting more than 50bp, have been shown to encompass a significant portion of the genome and can have large phenotypic effects. Additionally, increasing empirical evidence demonstrates that structural variants may play a substantial role in speciation, which could previously have been overlooked because of difficulties in identifying them with short-read data. However, with the increased availability of long-read sequencing technology we are now equipped better than ever to address this limitation and study the contribution of different types of structural variants to genetic variation within and genetic differentiation between closely related species. Here, we follow this approach and combine PacBio HiFi and HiC sequencing for two closely related passerine birds, the collared flycatcher and the pied flycatcher. This enables us to generate a chromosome-level genome assembly for both species, and identify structural variants between the two species. Based on population-level HiFi sequencing for both species, we then investigate patterns of single nucleotide diversity and differentiation within and between species and their association with different types of structural variation. We find widespread structural variation between the two species, where both the sex chromosomes show a disproportionate number of structural variants, which may help explain the suspected role of the Z-chromosome in contributing to genetic incompatibilities. We also find that genomic differentiation peaks are enriched in both translocations and inversions, which supports a mechanistic role of structural variation in population differentiation and speciation.
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| 2. |
- Cramer, Emily R. A., et al.
(author)
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Females discriminate against heterospecific sperm in a natural hybrid zone
- 2016
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In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 70:8, s. 1844-1855
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Journal article (peer-reviewed)abstract
- 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.
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| 3. |
- Kawakami, Takeshi, et al.
(author)
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Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array
- 2014
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In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 14:6, s. 1248-1260
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Journal article (peer-reviewed)abstract
- 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.
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| 4. |
- McFarlane, S. Eryn, et al.
(author)
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Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister species
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Journal article (peer-reviewed)abstract
- 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.
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| 5. |
- McFarlane, S. Eryn, et al.
(author)
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Difference in plasticity of resting metabolic rate - the proximate explanation to different niche breadth in sympatric Ficedula flycatchers
- 2018
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 8:9, s. 4575-4586
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Journal article (peer-reviewed)abstract
- 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.
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| 6. |
- McFarlane, S. Eryn, et al.
(author)
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Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers
- 2016
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In: PLOS ONE. - : Public Library of Science (PLoS). - 1932-6203. ; 11:9
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Journal article (peer-reviewed)abstract
- 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.
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| 7. |
- McFarlane, S. Eryn, et al.
(author)
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Low Heritability but Significant Early Environmental Effects on Resting Metabolic Rate in a Wild Passerine
- 2021
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In: American Naturalist. - : University of Chicago Press. - 0003-0147 .- 1537-5323. ; 198:4, s. 551-560
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Journal article (peer-reviewed)abstract
- Predicting the impact of climate change on biodiversity requires understanding the adaptation potential of wild organisms. Evolutionary responses depend on the additive genetic variation associated with the phenotypic traits targeted by selection. We combine 5 years of cross-fostering experiments, measurements of resting metabolic rate (RMR) on nearly 200 wild collared flycatcher (Ficedula albicollis) nestlings, and animal models using a 17-year pedigree to evaluate the potential for an evolutionary response to changing environmental conditions. Contrary to other avian studies, we find no significant heritability of whole-organism, mass-independent, or mass-specific RMR, but we report a strong effect of nest environment instead. We therefore conclude that variation in nestling RMR is explained by variation in the early-life environment provided by the parents. We discuss possible underlying specific parental effects and the importance of taking different mechanisms into account to understand how animals phenotypically adapt (or fail to adapt) to climate change.
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| 8. |
- McFarlane, S. Eryn, et al.
(author)
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RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair
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Other publication (other academic/artistic)abstract
- 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
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| 9. |
- McFarlane, S. Eryn, et al.
(author)
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Sexual selection affects climate adaptation in collared flycatchers
- 2017
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Other publication (other academic/artistic)abstract
- 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.
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| 10. |
- McFarlane, S. Eryn, et al.
(author)
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Sexual selection affects climate adaptation in collared flycatchers
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Journal article (peer-reviewed)abstract
- 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.
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