1. |
- Silva, C. N. S., et al.
(author)
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Insights into the genetic architecture of morphological traits in two passerine bird species
- 2017
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In: Heredity. - : Springer Science and Business Media LLC. - 0018-067X .- 1365-2540. ; 119:3, s. 197-205
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Journal article (peer-reviewed)abstract
- 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.
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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. |
- Kardos, Marty, et al.
(author)
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Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations
- 2016
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In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 16:3, s. 727-741
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Journal article (peer-reviewed)abstract
- 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.
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4. |
- Lane, Jeffrey E., et al.
(author)
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Phenological shifts in North American red squirrels : disentangling the roles of phenotypic plasticity and microevolution
- 2018
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In: Journal of Evolutionary Biology. - : WILEY. - 1010-061X .- 1420-9101. ; 31:6, s. 810-821
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Journal article (peer-reviewed)abstract
- Phenological shifts are the most widely reported ecological responses to climate change, but the requirements to distinguish their causes (i.e. phenotypic plasticity vs. microevolution) are rarely met. To do so, we analysed almost two decades of parturition data from a wild population of North American red squirrels (Tamiasciurus hudsonicus). Although an observed advance in parturition date during the first decade provided putative support for climate change-driven microevolution, a closer look revealed a more complex pattern. Parturition date was heritable [h(2)=0.14 (0.07-0.21 (HPD interval)] and under phenotypic selection [=-0.14 +/- 0.06 (SE)] across the full study duration. However, the early advance reversed in the second decade. Further, selection did not act on the genetic contribution to variation in parturition date, and observed changes in predicted breeding values did not exceed those expected due to genetic drift. Instead, individuals responded plastically to environmental variation, and high food [white spruce (Picea glauca) seed] production in the first decade appears to have produced a plastic advance. In addition, there was little evidence of climate change affecting the advance, as there was neither a significant influence of spring temperature on parturition date or evidence of a change in spring temperatures across the study duration. Heritable traits not responding to selection in accordance with quantitative genetic predictions have long presented a puzzle to evolutionary ecologists. Our results on red squirrels provide empirical support for one potential solution: phenotypic selection arising from an environmental, as opposed to genetic, covariance between the phenotypic trait and annual fitness.
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5. |
- McFarlane, S. Eryn, et al.
(author)
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Detecting the True Extent of Introgression during Anthropogenic Hybridization
- 2019
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In: Trends in Ecology and Evolution. - : Elsevier BV. - 0169-5347. ; 34:4, s. 315-326
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Journal article (peer-reviewed)abstract
- Hybridization among naturally separate taxa is increasing owing to human impact, and can result in taxon loss. Previous classification of anthropogenic hybridization has largely ignored the case of bimodal hybrid zones, in which hybrids commonly mate with parental species, resulting in many backcrossed individuals with a small proportion of introgressed genome. Genetic markers can be used to detect such hybrids, but until recently too few markers have been used to detect the true extent of introgression. Recent studies of wolves and trout have employed thousands of markers to reveal previously undetectable backcrosses. This improved resolution will lead to increased detection of late-generation backcrosses, shed light on the consequences of anthropogenic hybridization, and pose new management issues for conservation scientists.
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6. |
- 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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7. |
- 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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8. |
- 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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9. |
- McFarlane, S. Eryn, et al.
(author)
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Song discrimination by nestling collared flycatchers during early development
- 2016
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In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 12:7
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Journal article (peer-reviewed)abstract
- Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatty with closely related species.
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10. |
- McFarlane, S. Eryn, 1988-
(author)
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Speciation and Metabolic rate : Insights from an avian hybrid zone
- 2017
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Doctoral thesis (other academic/artistic)abstract
- 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.
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