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When populations colonise new environments, they may be exposed to novel selection pressures but also suffer from extensive genetic drift due to founder effects, small population sizes and limited interpopulation gene flow. Genomic approaches enable us to study how these factors drive divergence, and disentangle neutral effects from differentiation at specific loci due to selection. Here, we investigate patterns of genetic diversity and divergence using whole-genome resequencing (>22× coverage) in Berthelot's pipit (Anthus berthelotii), a passerine endemic to the islands of three north Atlantic archipelagos. Strong environmental gradients, including in pathogen pressure, across populations in the species range, make it an excellent system in which to explore traits important in adaptation and/or incipient speciation. First, we quantify how genomic divergence accumulates across the speciation continuum, that is, among Berthelot's pipit populations, between sub species across archipelagos, and between Berthelot's pipit and its mainland ancestor, the tawny pipit (Anthus campestris). Across these colonisation timeframes (2.1 million-ca. 8000 years ago), we identify highly differentiated loci within genomic islands of divergence and conclude that the observed distributions align with expectations for non-neutral divergence. Characteristic signatures of selection are identified in loci associated with craniofacial/bone and eye development, metabolism and immune response between population comparisons. Interestingly, we find limited evidence for repeated divergence of the same loci across the colonisation range but do identify different loci putatively associated with the same biological traits in different populations, likely due to parallel adaptation. Incipient speciation across these island populations, in which founder effects and selective pressures are strong, may therefore be repeatedly associated with morphology, metabolism and immune defence., (© 2024 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology and migratory behaviour, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from five taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked whether these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g. areas of low recombination). Consequently, studies employing genome scans to search for areas important for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation., (© 2017 John Wiley & Sons Ltd.)

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty-seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab-raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free-living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free-living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5-5.8% of the total variance-a large effect for a single gene influencing a complex behavioural trait-but not in three others. The confirmation of an association between SNP830 genotype and personality-related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.

The timing of reproduction in birds varies considerably within populations and is often under strong natural selection. Individual timing within years is dependent on a range of environmental factors in addition to having an additive genetic basis. In vertebrates, an increasing amount is known about the molecular basis for variation in biological timing. The Clock gene includes a variable poly-glutamine (poly-Q) repeat influencing behaviour and physiology. Recent work in birds, fish and insects has demonstrated associations between Clock genotype and latitude across populations, which match latitudinal variation in breeding time. In this study, we investigated the phenotypic correlates of variation in Clock genotype within a single blue tit Cyanistes caeruleus population over two successive breeding seasons. In females, but not in males, we observed a general trend for birds with fewer poly-Q repeats to breed earlier in the season. Incubation duration was shorter in both females and males with fewer repeats at the polymorphic Clock locus. Poly-Q Clock allele-frequency was homogenously distributed within the study population and did not exhibit any consistent environment-related variation. We further tested for effects of Clock genotype on reproductive success and survival, and found that females with fewer poly-Q repeats produced a higher number of fledged offspring. Our results therefore suggest that (i) selection in females, but not in males, for fewer poly-Q repeats may be operating, (ii) the across-population associations in timing of breeding involving this locus could be linked to variation within populations, and (iii) the Clock gene might be involved in local adaptation to seasonal environments.

The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape., (© 2023 John Wiley & Sons Ltd.)

The seasonal migration of birds is a fascinating natural wonder. Avian migratory behaviour changes are common and are probably a polygenic process as avian migration is governed by multiple correlated components with a variable genetic basis. However, the genetic and phenotypic changes involving migration changes are poorly studied. Using one annotated near-chromosomal level de novo genome assembly, 50 resequenced genomes, hundreds of morphometric data and species distribution information, we investigated population structure and genomic and phenotypic differences associated with differences in migratory behaviour in a songbird species, Yellow-throated Bunting Emberiza elegans (Aves: Emberizidae). Population genomic analyses reveal extensive gene flow between the southern resident and the northern migratory populations of this species. The hand-wing index is significantly lower in the resident populations than in the migratory populations, indicating reduced flight efficiency of the resident populations. Here, we discuss the possibility that nonmigratory populations may have originated from migratory populations though migration loss. We further infer that the alterations of genes related to energy metabolism, nervous system and circadian rhythm may have played major roles in regulating migration change. Our study sheds light on phenotypic and polygenic changes involving migration change., (© 2022 John Wiley & Sons Ltd.)

Migration in animals and associated adaptations to contrasting environments are underpinned by complex genetic architecture. Here, we explore the genomic basis of facultative anadromy in brown trout (Salmo trutta), wherein some individuals migrate to sea while others remain resident in natal rivers, to better understand how alternative migratory tactics (AMTs) are maintained evolutionarily. To identify genomic variants associated with AMTs, we sequenced whole genomes for 194 individual trout from five anadromous-resident population pairs, situated above and below waterfalls, in five different Irish rivers. These waterfalls act as natural barriers to upstream migration and hence we predicted that loci underpinning AMTs should be under similar divergent selection across these replicate pairs. A sliding windows based analysis revealed a highly polygenic adaptive divergence between anadromous and resident populations, encompassing 329 differentiated genomic regions. These regions were associated with 292 genes involved in various processes crucial for AMTs, including energy homeostasis, reproduction, osmoregulation, immunity, circadian rhythm and neural function. Furthermore, examining patterns of diversity we were able to link specific genes and biological processes to putative AMT trait classes: migratory-propensity, migratory-lifestyle and residency. Importantly, AMT outlier regions possessed higher genetic diversity than the background genome, particularly in the anadromous group, suggesting balancing selection may play a role in maintaining genetic variation. Overall, the results from this study provide important insights into the genetic architecture of migration and the evolutionary mechanisms shaping genomic diversity within and across populations., (© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.)

The genetic basis of bird migration has been the focus of several studies. Two willow warbler subspecies (Phylloscopus trochilus trochilus and Phylloscopus trochilus acredula) follow different migratory routes to wintering grounds in Africa. Their breeding populations overlap in contact areas or "migratory divides" located in central Scandinavia and in eastern Poland. Earlier analyses demonstrated that the genetic differences between these two migratory phenotypes are few and cluster on chromosomes 1 and 5. In addition, an amplified fragment length polymorphism-derived biallelic marker (known as WW2) presents steep clines across both migratory divides but failed to be mapped in the genome. Here, we characterize the WW2 marker and describe its two variants (WW2 ancestral and WW2 derived) as portions of long terminal repeat retrotransposons originating from an ancient infection by an endogenous retrovirus. We used quantitative polymerase chain reaction techniques to quantify copy numbers of the WW2 derived variant in the two subspecies and their hybrids. This, together with genome analyses revealed that WW2 derived variants are much more abundant in P. t. acredula and appear embedded in a large repeat-rich region (>12 Mbp), not associated with the divergent regions of chromosomes 1 or 5. However, it might interact with genetic elements controlling migration direction. Testing this hypothesis further will require knowing the exact location of this region, such as by obtaining more complete genome assemblies preferably in combination with techniques like fluorescence in situ hybridization applied to a willow warbler karyotype, and finally to investigate the copy number of this marker in hybrids with known migratory tracks., (© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Population genomics applied to game species conservation can help delineate management units, ensure appropriate harvest levels and identify populations needing genetic rescue to safeguard their adaptive potential. The ruffed grouse (Bonasa umbellus) is rapidly declining in much of the eastern USA due to a combination of forest maturation and habitat fragmentation. More recently, mortality from West Nile Virus may have affected connectivity of local populations; however, genetic approaches have never explicitly investigated this issue. In this study, we sequenced 54 individual low‐coverage (~5X) grouse genomes to characterize population structure, assess migration rates across the landscape to detect potential barriers to gene flow and identify genomic regions with high differentiation. We identified two genomic clusters with no clear geographic correlation, with large blocks of genomic differentiation associated with chromosomes 4 and 20, likely due to chromosomal inversions. After excluding these putative inversions from the data set, we found weak but nonsignificant signals of population subdivision. Estimated gene flow revealed reduced rates of migration in areas with extensive habitat fragmentation and increased genetic connectivity in areas with less habitat fragmentation. Our findings provide a benchmark for wildlife managers to compare and scale the genetic diversity and structure of ruffed grouse populations in Pennsylvania and across the eastern USA, and we also reveal structural variation in the grouse genome that requires further study to understand its possible effects on individual fitness and population distribution. [ABSTRACT FROM AUTHOR]

Despite receiving significant recent attention, the relevance of structural variation (SV) in driving phenotypic diversity remains understudied, although recent advances in long-read sequencing, bioinformatics and pangenomic approaches have enhanced SV detection. We review the role of SVs in shaping phenotypes in avian model systems, and identify some general patterns in SV type, length and their associated traits. We found that most of the avian SVs so far identified are short indels in chickens, which are frequently associated with changes in body weight and plumage colouration. Overall, we found that relatively short SVs are more frequently detected, likely due to a combination of their prevalence compared to large SVs, and a detection bias, stemming primarily from the widespread use of short-read sequencing and associated analytical methods. SVs most commonly involve non-coding regions, especially introns, and when patterns of inheritance were reported, SVs associated primarily with dominant discrete traits. We summarise several examples of phenotypic convergence across different species, mediated by different SVs in the same or different genes and different types of changes in the same gene that can lead to various phenotypes. Complex rearrangements and supergenes, which can simultaneously affect and link several genes, tend to have pleiotropic phenotypic effects. Additionally, SVs commonly co-occur with single-nucleotide polymorphisms, highlighting the need to consider all types of genetic changes to understand the basis of phenotypic traits. We end by summarising expectations for when long-read technologies become commonly implemented in non-model birds, likely leading to an increase in SV discovery and characterisation. The growing interest in this subject suggests an increase in our understanding of the phenotypic effects of SVs in upcoming years., (© 2024 John Wiley & Sons Ltd.)

Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations and drive speciation. Across island systems, contemporary patterns of genetic diversity reflect population demography, including colonization events, bottlenecks, gene flow and genetic drift. Here, we investigate genome‐wide diversity and the distribution of runs of homozygosity (ROH) using whole‐genome resequencing of individuals (>22× coverage) from six populations across three archipelagos of Berthelot's pipit (Anthus berthelotii)‐a passerine that has recently undergone island speciation. We show the most dramatic reduction in diversity occurs between the mainland sister species (the tawny pipit) and Berthelot's pipit and is lowest in the populations that have experienced sequential bottlenecks (i.e., the Madeiran and Selvagens populations). Pairwise sequential Markovian coalescent (PSMC) analyses estimated that Berthelot's pipit diverged from its sister species ~2 million years ago, with the Madeiran archipelago founded 50,000 years ago, and the Selvagens colonized 8000 years ago. We identify many long ROH (>1 Mb) in these most recently colonized populations. Population expansion within the last 100 years may have eroded long ROH in the Madeiran archipelago, resulting in a prevalence of short ROH (<1 Mb). However, the extensive long and short ROH detected in the Selvagens suggest strong recent inbreeding and bottleneck effects, with as much as 38% of the autosomes consisting of ROH >250 kb. These findings highlight the importance of demographic history, as well as selection and genetic drift, in shaping contemporary patterns of genomic diversity across diverging populations. [ABSTRACT FROM AUTHOR]

The term "haplotype block" is commonly used in the developing field of haplotype‐based inference methods. We argue that the term should be defined based on the structure of the Ancestral Recombination Graph (ARG), which contains complete information on the ancestry of a sample. We use simulated examples to demonstrate key features of the relationship between haplotype blocks and ancestral structure, emphasizing the stochasticity of the processes that generate them. Even the simplest cases of neutrality or of a "hard" selective sweep produce a rich structure, often missed by commonly used statistics. We highlight a number of novel methods for inferring haplotype structure, based on the full ARG, or on a sequence of trees, and illustrate how they can be used to define haplotype blocks using an empirical data set. While the advent of new, computationally efficient methods makes it possible to apply these concepts broadly, they (and additional new methods) could benefit from adding features to explore haplotype blocks, as we define them. Understanding and applying the concept of the haplotype block will be essential to fully exploit long and linked‐read sequencing technologies. [ABSTRACT FROM AUTHOR]

Migratory insects are capable of actively sustaining powered flight for several hours. This extraordinary phenomenon requires a highly efficient transport system to cope with the energetic demands placed on the flight muscles. Here, we provide evidence that the role of the hydrophobic ligand binding of odorant binding proteins (OBPs) extends beyond their typical function in the olfactory system to support insect flight activity via lipid interactions. Transcriptomic and candidate gene analyses show that two phylogenetically clustered OBPs (OBP3/OBP6) are consistently over-expressed in adult moths of the migrant Old-World bollworm, Helicoverpa armigera, displaying sustained flight performance in flight activity bioassays. Tissue-specific over-expression of OBP6 was observed in the antennae, wings and thorax in long-fliers of H. armigera. Transgenic Drosophila flies over-expressing an H. armigera transcript of OBP6 (HarmOBP6) in the flight muscle attained higher flight speeds on a modified tethered flight system. Quantification of lipid molecules using mass spectrometry showed a depletion of triacylglyerol and phospholipids in flown moths. Protein homology models built from the crystal structure of a fatty acid carrier protein identified the binding site of OBP3 and OBP6 for hydrophobic ligand binding with both proteins exhibiting a stronger average binding affinity with triacylglycerols and phospholipids compared with other groups of ligands. We propose that HarmOBP3 and HarmOBP6 contribute to the flight capacity of a globally invasive and highly migratory noctuid moth, and in doing so, extend the function of this group of proteins beyond their typical role as chemosensory proteins in insects., (© 2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Increasing our understanding of how evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, genome-wide patterns of within- and between- species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole-genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories and investigate patterns of diversity and divergence within and between species. Using Populus trichocarpa as an outgroup species, we further infer the genealogical relationships and estimate the extent of ancient introgression among the three aspen species (Populus tremula, Populus davidiana and Populus tremuloides) throughout the genome. Our results show substantial variation in these patterns along the genomes with this variation being strongly predicted by local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long-term balancing selection have also been crucial components in shaping patterns of genome-wide variation during the speciation process., (© 2020 John Wiley & Sons Ltd.)

Understanding the mechanisms underlying heterogeneous genomic divergence is of particular interest in evolutionary biology. Highly differentiated genomic regions, known as genomic islands, often evolve between diverging lineages. These genomic islands may be related to selection promoting adaptation or reproductive isolation. Based on whole genome assembly and genome‐wide RAD sequencing in a pair of yellow croakers (genus: Larimichthys), we investigated the evolutionary processes shaping genomic landscapes of divergence. Demographic modelling indicated that the two species diverged following a secondary contact scenario, where differential introgression and linked selection were suggested to be involved in heterogeneous genomic divergence. We identified reduced recombination rate in genomic islands and a relatively good conservation of both genetic diversity and recombination landscapes between species, which highlight the roles of linked selection and recombination rate variation in promoting heterogeneous divergence in the common ancestral lineage of the two species. In addition, we found a positive correlation between differentiation (FST) and absolute sequence divergence (Dxy), and elevated Dxy in genomic islands, indicating that the genomic landscape of divergence was not shaped by linked selection alone. Restricted gene flow in highly differentiated regions has probably remodelled the landscape of heterogeneous genomic divergence. This study highlights that highly differentiated genomic regions can also arise from a combination of linked selection and differential gene flow in interaction with varying recombination rates. [ABSTRACT FROM AUTHOR]

Insects are capable of extraordinary feats of long‐distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high‐quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome‐wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non‐migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life‐history strategy. [ABSTRACT FROM AUTHOR]

We investigated the potential mechanisms driving habitat‐linked genetic divergence within a bird species endemic to a single 250‐km2 island. The island scrub‐jay (Aphelocoma insularis) exhibits microgeographic divergence in bill morphology across pine–oak ecotones on Santa Cruz Island, California (USA), similar to adaptive differences described in mainland congeners over much larger geographic scales. To test whether individuals exhibit genetic differentiation related to habitat type and divergence in bill length, we genotyped over 3000 single nucleotide polymorphisms in 123 adult island scrub‐jay males from across Santa Cruz Island using restriction site‐associated DNA sequencing. Neutral landscape genomic analyses revealed that genome‐wide genetic differentiation was primarily related to geographic distance and differences in habitat composition. We also found 168 putatively adaptive loci associated with habitat type using multivariate redundancy analysis while controlling for spatial effects. Finally, two genome‐wide association analyses revealed a polygenic basis to variation in bill length with multiple loci detected in or near genes known to affect bill morphology in other birds. Our findings support the hypothesis that divergent selection at microgeographic scales can cause adaptive divergence in the presence of ongoing gene flow. [ABSTRACT FROM AUTHOR]

Present‐day ecology and population structure are the legacies of past climate and habitat perturbations, and this is particularly true for species that are widely distributed at high latitudes. The red knot, Calidris canutus, is an arctic‐breeding, long‐distance migratory shorebird with six recognized subspecies defined by differences in morphology, migration behavior, and annual cycle phenology, in a global distribution thought to have arisen just since the last glacial maximum (LGM). We used nextRAD sequencing of 10,881 single‐nucleotide polymorphisms (SNPs) to assess the neutral genetic structure and phylogeographic history of 172 red knots representing all known global breeding populations. Using population genetics approaches, including model‐based scenario‐testing in an approximate Bayesian computation (ABC) framework, we infer that red knots derive from two main lineages that diverged ca. 34,000 years ago, and thus most probably persisted at the LGM in both Palearctic and Nearctic refugia, followed by at least two instances of secondary contact and admixture. Within two Beringian subspecies (C. c. roselaari and rogersi), we detected previously unknown genetic structure among sub‐populations sharing a migratory flyway, reflecting additional complexity in the phylogeographic history of the region. Conversely, we found very weak genetic differentiation between two Nearctic populations (rufa and islandica) with clearly divergent migratory phenotypes and little or no apparent contact throughout the annual cycle. Together, these results suggest that relative gene flow among migratory populations reflects a complex interplay of historical, geographical, and ecological factors. [ABSTRACT FROM AUTHOR]

Chromosomal inversions are known to play roles in adaptation and differentiation in many species. They involve clusters of correlated genes (i.e., loci in linkage disequilibrium, LD) possibly associated with environmental variables. The grasshopper "species complex" Trimerotropis pallidipennis comprises several genetic lineages distributed from North to South America in arid and semi‐arid high‐altitude environments. The southernmost lineage, Trimerotropis sp., segregates for four to seven putative inversions that display clinal variation, possibly through adaptation to temperate environments. We analysed chromosomal, mitochondrial and genome‐wide single nucleotide polymorphism data in 19 Trimerotropis sp. populations mainly distributed along two altitudinal gradients (MS and Ju). Populations across Argentina comprise two main chromosomally and genetically differentiated lineages: one distributed across the southernmost border of the "Andes Centrales," adding evidence for a differentiation hotspot in this area; and the other widely distributed in Argentina. Within the latter, network analytical approaches to LD found three clusters of correlated loci (LD‐clusters), with inversion karyotypes explaining >79% of the genetic variation. Outlier loci associated with environmental variables mapped to two of these LD‐clusters. Furthermore, despite the complex geographical history indicated by population genetic analyses, the clines in inversion karyotypes have remained stable for more than 20 generations, implicating their role in adaptation and differentiation within this lineage. We hypothesize that these clines could be the consequence of a coupling between extrinsic postzygotic barriers and spatially varying selection along environmental gradients resulting in a hybrid zone. These results provide a framework for future investigations about candidate genes implicated in rapid adaptation to new environments. [ABSTRACT FROM AUTHOR]

Morphological differentiation associated with evolutionary diversification is often explained with adaptive benefits but the processes and mechanisms maintaining cryptic diversity are still poorly understood. Using genome‐wide data, we show here that the pale sand martin Riparia diluta in Central and East Asia consists of three genetically deeply differentiated lineages which vary only gradually in morphology but broadly reflect traditional taxonomy. We detected no signs of gene flow along the eastern edge of the Qinghai‐Tibetan plateau between lowland south‐eastern Chinese R. d. fohkienensis and high‐altitude R. d. tibetana. Largely different breeding and migration timing between these low and high altitude populations as indicated by phenology data suggests that allochrony might act as prezygotic isolation mechanism in the area where their ranges abut. Mongolian populations of R. d. tibetana, however, displayed signs of limited mixed ancestries with Central Asian R. d. diluta. Their ranges meet in the area of a well‐known avian migratory divide, where western lineages take a western migration route around the Qinghai‐Tibetan plateau to winter quarters in South Asia, and eastern lineages take an eastern route to Southeast Asia. This might also be the case between western R. d. diluta and eastern R. d. tibetana as indicated by differing wintering grounds. We hypothesize that hybrids might have nonoptimal intermediate migration routes and selection against them might restrict gene flow. Although further potential isolation mechanisms might exist in the pale sand martin, our study points towards contrasting migration behaviour as an important factor in maintaining evolutionary diversity under morphological stasis. [ABSTRACT FROM AUTHOR]

Populations are under strong selection to match reproductive timing with favourable environmental conditions. This becomes particularly important and challenging with increasing interannual environmental variability. Adjusting reproductive timing requires the ability to sense and interpret relevant environmental cues, while responding flexibly to their interannual variation. For instance, in seasonal species, reproductive timing is often dependent on photoperiod and temperature. Although many genes influencing the timing of reproduction have been identified, far less attention has been paid to the gene‐regulatory cascades orchestrating these complex gene‐environment interactions. In a From the Cover article in this issue of Molecular Ecology, Lindner, Laine, et al. (2021) addressed this knowledge gap by investigating the role of DNA methylation in mediating reproductive timing in the seasonally breeding great tit (Parus major). Using a clever blood sampling design, they investigated genome‐wide DNA methylation changes following individual female birds across multiple reproductive stages. This approach revealed 10 candidate genes with a strong correlation between promoter methylation and reproductive status. Some of these genes are known to be involved in reproductive timing (e.g., MYLK‐like or NR5A1), yet for others this function was previously unknown (Figure 1). Interestingly, NR5A1 is a key transcription factor, which may affect other genes that are part of the same regulatory network. The findings of Lindner, Laine, et al. (2021) provide a strong case for studying DNA methylation to uncover how gene‐environment interactions influence important life‐history traits, such as reproductive timing. [ABSTRACT FROM AUTHOR]

Clock genes exhibit substantial control over gene expression and ultimately life‐histories using external cues such as photoperiod, and are thus likely to be critical for adaptation to shifting seasonal conditions and novel environments as species redistribute their ranges under climate change. Coding trinucleotide repeats (cTNRs) are found within several clock genes, and may be interesting targets of selection due to their containment within exonic regions and elevated mutation rates. Here, we conduct inter‐specific characterization of the NR1D1 cTNR between Canada lynx and bobcat, and intra‐specific spatial and environmental association analyses of neutral microsatellites and our functional cTNR marker, to investigate the role of selection on this locus in Canada lynx. We report signatures of divergent selection between lynx and bobcat, with the potential for hybrid‐mediated gene flow in the area of range overlap. We also provide evidence that this locus is under selection across Canada lynx in eastern Canada, with both spatial and environmental variables significantly contributing to the explained variation, after controlling for neutral population structure. These results suggest that cTNRs may play an important role in the generation of functional diversity within some mammal species, and allow for contemporary rates of adaptation in wild populations in response to environmental change. We encourage continued investment into the study of cTNR markers to better understand their broader relevance to the evolution and adaptation of mammals. [ABSTRACT FROM AUTHOR]

Determining how genetic diversity is structured between populations that span the divergence continuum from populations to biological species is key to understanding the generation and maintenance of biodiversity. We investigated genetic divergence and gene flow in eight lineages of birds with a trans‐Beringian distribution, where Asian and North American populations have likely been split and reunited through multiple Pleistocene glacial cycles. Our study transects the speciation process, including eight pairwise comparisons in three orders (ducks, shorebirds and passerines) at population, subspecies and species levels. Using ultraconserved elements (UCEs), we found that these lineages represent conditions from slightly differentiated populations to full biological species. Although allopatric speciation is considered the predominant mode of divergence in birds, all of our best divergence models included gene flow, supporting speciation with gene flow as the predominant mode in Beringia. In our eight lineages, three were best described by a split‐migration model (divergence with gene flow), three best fit a secondary contact scenario (isolation followed by gene flow), and two showed support for both models. The lineages were not evenly distributed across a divergence space defined by gene flow (M) and differentiation (FST), instead forming two discontinuous groups: one with relatively shallow divergence, no fixed single nucleotide polymorphisms (SNPs), and high rates of gene flow between populations; and the second with relatively deeply divergent lineages, multiple fixed SNPs, and low gene flow. Our results highlight the important role that gene flow plays in avian divergence in Beringia. [ABSTRACT FROM AUTHOR]

Understanding the origin of new species is a central goal in evolutionary biology. Diverging lineages often evolve highly heterogeneous patterns of genetic differentiation; however, the underlying mechanisms are not well understood. We investigated evolutionary processes governing genetic differentiation between the hybridizing campions Silene dioica (L.) Clairv. and S. latifolia Poiret. Demographic modelling indicated that the two species diverged with gene flow. The best‐supported scenario with heterogeneity in both migration rate and effective population size suggested that a small proportion of the loci evolved without gene flow. Differentiation (FST) and sequence divergence (dXY) were correlated and both tended to peak in the middle of most linkage groups, consistent with reduced gene flow at highly differentiated loci. Highly differentiated loci further exhibited signatures of selection. In between‐species population pairs, isolation by distance was stronger for genomic regions with low between‐species differentiation than for highly differentiated regions that may contain barrier loci. Moreover, differentiation landscapes within and between species were only weakly correlated, suggesting that linked selection due to shared recombination and gene density landscapes is not the dominant determinant of genetic differentiation in these lineages. Instead, our results suggest that divergent selection shaped the genomic landscape of differentiation between the two Silene species, consistent with predictions for speciation in the face of gene flow. [ABSTRACT FROM AUTHOR]

Investigating the relative importance of neutral versus selective processes governing the accumulation of genetic variants is a key goal in both evolutionary and conservation biology. This is particularly true in the context of small populations, where genetic drift can counteract the effect of selection. Using Brook Charr (Salvelinus fontinalis) from Québec, Canada, as a case study, we investigated the importance of demographic versus selective processes governing the accumulation of both adaptive and maladaptive mutations in closed versus open and connected populations to assess gene flow effect. This was achieved by using 14,779 high‐quality filtered SNPs genotyped among 1,416 fish representing 50 populations from three life history types: lacustrine (closed populations), riverine and anadromous (connected populations). Using the PROVEAN algorithm, we observed a considerable accumulation of putative deleterious mutations across populations. The absence of correlation between the occurrence of putatively beneficial or deleterious mutations and local recombination rate supports the hypothesis that genetic drift might be the main driver of the accumulation of such variants. However, despite a lower genetic diversity observed in lacustrine than in riverine or anadromous populations, lacustrine populations do not exhibit more deleterious mutations than the two other history types, suggesting that the negative effect of genetic drift in lacustrine populations may be mitigated by that of relaxed purifying selection. Moreover, we also identified genomic regions associated with anadromy, as well as an overrepresentation of transposable elements associated with variation in environmental variables, thus supporting the importance of transposable elements in adaptation. [ABSTRACT FROM AUTHOR]

Monarch butterflies are known for their spectacular annual migration in eastern North America, with millions of monarchs flying up to 4,500 km to overwintering sites in central Mexico. Monarchs also live west of the Rocky Mountains, where they travel shorter distances to overwinter along the Pacific Coast. It is often assumed that eastern and western monarchs form distinct evolutionary units, but genomic studies to support this notion are lacking. We used a tethered flight mill to show that migratory eastern monarchs have greater flight performance than western monarchs, consistent with their greater migratory distances. However, analysing more than 20 million SNPs in 43 monarch genomes, we found no evidence for genomic differentiation between eastern and western monarchs. Genomic analysis also showed identical and low levels of genetic diversity, and demographic analyses indicated similar effective population sizes and ongoing gene flow between eastern and western monarchs. Gene expression analysis of a subset of candidate genes during active flight revealed differential gene expression related to nonmuscular motor activity. Our results demonstrate that eastern and western monarchs maintain migratory differences despite ongoing gene flow, and suggest that migratory differences between eastern and western monarchs are not driven by select major‐effects alleles. Instead, variation in migratory distance and destination may be driven by environmentally induced differential gene expression or by many alleles of small effect. [ABSTRACT FROM AUTHOR]

Species inhabiting marine environments face a wide range of environmental conditions that vary spatially across several orders of magnitude. The selective pressures that these conditions impose on marine organisms, in combination with potentially high rates of gene flow between distant populations, make it difficult to predict the extent to which these populations can locally adapt. Here, I identify how selection and gene flow influence the population genetic structure of the anemone Anthopleura elegantissima along the Pacific coast of North America. Isolation by distance is the dominant pattern across the range of this species, with a genetic break near Pt. Conception, CA. Furthermore, demographic modelling suggests that this species was historically confined to southerly latitudes before expanding northward. Outlier analyses identify 24 loci under selection (out of ~1,100), but the same analysis on simulated genetic data generated using the most likely demographic model erroneously identified the same number of loci under selection, if not more. Taken together, these results suggest that demographic processes are the dominant force shaping population genetic patterns in A. elegantissima along the Pacific coast of North America. I discuss these patterns in terms of the evolutionary history of A. elegantissima, the potential for local adaptation, and their consequences with respect to interactions with the endosymbiont Breviolum muscatinei across their geographic range. [ABSTRACT FROM AUTHOR]

Landscape permeability is often explored spatially, but may also vary temporally. Landscape permeability, including partial barriers, influences migratory animals that move across the landscape. Partial barriers are common in rivers where barrier passage varies with streamflow. We explore the influence of partial barriers on the spatial and temporal distribution of migration‐linked genotypes of Oncorhynchus mykiss, a salmonid fish with co‐occurring resident and migratory forms, in tributaries to the South Fork Eel River, California, USA, Elder and Fox Creeks. We genotyped >4,000 individuals using RAD‐capture and classified individuals as resident, heterozygous or migratory genotypes using life history‐associated loci. Across four years of study (2014–2017), the permeability of partial barriers varied across dry and wet years. In Elder Creek, the largest waterfall was passable for adults migrating up‐river 4–39 days each year. In this stream, the overall spatial pattern, with fewer migratory genotypes above the waterfall, remained true across dry and wet years (67%–76% of migratory alleles were downstream of the waterfall). We also observed a strong relationship between distance upstream and proportion of migratory alleles. In Fox Creek, the primary barrier is at the mouth, and we found that the migratory allele frequency varied with the annual timing of high flow events. In years when rain events occurred during the peak breeding season, migratory allele frequency was high (60%–68%), but otherwise it was low (30% in two years). We highlight that partial barriers and landscape permeability can be temporally dynamic, and this effect can be observed through changing genotype frequencies in migratory animals. [ABSTRACT FROM AUTHOR]

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically‐determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally‐controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause‐inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin‐like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change. [ABSTRACT FROM AUTHOR]

Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large‐scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence—whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole‐genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)—a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST) regions generally had low genetic diversity (θπ), but increased absolute divergence (DXY) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression. [ABSTRACT FROM AUTHOR]

Patterns of genomic divergence between hybridizing taxa can be heterogeneous along the genome. Both differential introgression and local adaptation may contribute to this pattern. Here, we analysed two teosinte subspecies, Zea mays ssp. parviglumis and ssp. mexicana, to test whether their divergence has occurred in the face of gene flow and to infer which environmental variables have been important drivers of their ecological differentiation. We generated 9,780 DArTseqTM SNPs for 47 populations, and used an additional data set containing 33,454 MaizeSNP50 SNPs for 49 populations. With these data, we inferred features of demographic history and performed genome wide scans to determine the number of outlier SNPs associated with climate and soil variables. The two data sets indicate that divergence has occurred or been maintained despite continuous gene flow and/or secondary contact. Most of the significant SNP associations were to temperature and to phosphorus concentration in the soil. A large proportion of these candidate SNPs were located in regions of high differentiation that had been identified previously as putative inversions. We therefore propose that genomic differentiation in teosintes has occurred by a process of adaptive divergence, with putative inversions contributing to reduced gene flow between locally adapted populations. [ABSTRACT FROM AUTHOR]

Geographic range shifts can cause secondary contact and hybridization between closely related species, revealing mechanisms of species formation and integrity. These dynamics typically play out in restricted geographic regions, but highly vagile species may experience major distributional changes resulting in broad areas of contact. The Glossy Ibis (Plegadis falcinellus) is a dispersive waterbird of the Old World and Australia that colonized eastern North America in the early 19th century and came into contact with the native White‐faced Ibis (P. chihi). Putative hybrids between the two species have been observed across North America. To examine the population genomic consequences of this natural invasion, we sequenced 4,616 ultraconserved elements from 66 individuals sampled across the distributions of falcinellus, chihi, and the Puna Ibis (P. ridgwayi) of South America. We found genomic differentiation among the three species. Loci with high sequence divergence were often shared across all pairwise species comparisons, were associated with regions of high nucleotide diversity, and were concentrated on the Z chromosome. We detected signals of genetic admixture between chihi and falcinellus in individuals both near and far from their core area of sympatry. Genomic cline analyses revealed evidence of greater introgression into falcinellus from chihi, but we found little evidence for selection against hybrids. We also found signals of admixture between ridgwayi and South American populations of chihi. Our results indicate vagile species can experience pervasive introgression upon secondary contact, although we suggest these dynamics may be more ephemeral than the stable hybrid zones often observed in less dispersive organisms. [ABSTRACT FROM AUTHOR]

Theory predicts that structural genomic variants such as inversions can promote adaptive diversification and speciation. Despite increasing empirical evidence that adaptive divergence can be triggered by one or a few large inversions, the degree to which widespread genomic regions under divergent selection are associated with structural variants remains unclear. Here we test for an association between structural variants and genomic regions that underlie parallel host‐plant‐associated ecotype formation in Timema cristinae stick insects. Using mate‐pair resequencing of 20 new whole genomes we find that moderately sized structural variants such as inversions, deletions and duplications are widespread across the genome, being retained as standing variation within and among populations. Using 160 previously published, standard‐orientation whole genome sequences we find little to no evidence that the DNA sequences within inversions exhibit accentuated differentiation between ecotypes. In contrast, a formerly described large region of reduced recombination that harbours genes controlling colour‐pattern exhibits evidence for accentuated differentiation between ecotypes, which is consistent with differences in the frequency of colour‐pattern morphs between host‐associated ecotypes. Our results suggest that some types of structural variants (e.g., large inversions) are more likely to underlie adaptive divergence than others, and that structural variants are not required for subtle yet genome‐wide genetic differentiation with gene flow. [ABSTRACT FROM AUTHOR]

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream‐resident (fluvial), lake‐migrant (adfluvial) and ocean‐migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site‐associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity. [ABSTRACT FROM AUTHOR]

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole‐genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord‐type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord‐type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification. [ABSTRACT FROM AUTHOR]

Detailed evaluations of genomic variation between sister species often reveal distinct chromosomal regions of high relative differentiation (i.e., "islands of differentiation" in FST), but there is much debate regarding the causes of this pattern. We briefly review the prominent models of genomic islands of differentiation and compare patterns of genomic differentiation in three closely related pairs of New World warblers with the goal of evaluating support for the four models. Each pair (MacGillivray's/mourning warblers; Townsend's/black‐throated green warblers; and Audubon's/myrtle warblers) consists of forms that were likely separated in western and eastern North American refugia during cycles of Pleistocene glaciations and have now come into contact in western Canada, where each forms a narrow hybrid zone. We show strong differences between pairs in their patterns of genomic heterogeneity in FST, suggesting differing selective forces and/or differing genomic responses to similar selective forces among the three pairs. Across most of the genome, levels of within‐group nucleotide diversity (πWithin) are almost as large as levels of between‐group nucleotide distance (πBetween) within each pair, suggesting recent common ancestry and/or gene flow. In two pairs, a pattern of the FST peaks having low πBetween suggests that selective sweeps spread between geographically differentiated groups, followed by local differentiation. This "sweep‐before‐differentiation" model is consistent with signatures of gene flow within the yellow‐rumped warbler species complex. These findings add to our growing understanding of speciation as a complex process that can involve phases of adaptive introgression among partially differentiated populations. [ABSTRACT FROM AUTHOR]

Theory and empirical patterns suggest a disproportionate role for sex chromosomes in evolution and speciation. Focusing on ZW sex determination (females ZW, males ZZ; the system in birds, many snakes, and lepidopterans), I review how evolutionary dynamics are expected to differ between the Z, W and the autosomes, discuss how these differences may lead to a greater role of the sex chromosomes in speciation and use data from birds to compare relative evolutionary rates of sex chromosomes and autosomes. Neutral mutations, partially or completely recessive beneficial mutations, and deleterious mutations under many conditions are expected to accumulate faster on the Z than on autosomes. Sexually antagonistic polymorphisms are expected to arise on the Z, raising the possibility of the spread of preference alleles. The faster accumulation of many types of mutations and the potential for complex evolutionary dynamics of sexually antagonistic traits and preferences contribute to a role for the Z chromosome in speciation. A quantitative comparison among a wide variety of bird species shows that the Z tends to have less within‐population diversity and greater between‐species differentiation than the autosomes, likely due to both adaptive evolution and a greater rate of fixation of deleterious alleles. The W chromosome also shows strong potential to be involved in speciation, in part because of its co‐inheritance with the mitochondrial genome. While theory and empirical evidence suggest a disproportionate role for sex chromosomes in speciation, the importance of sex chromosomes is moderated by their small size compared to the whole genome. [ABSTRACT FROM AUTHOR]

Abstract: Host specialization is a key process in ecological divergence and speciation of plant‐associated fungi. The underlying determinants of host specialization are generally poorly understood, especially in endophytes, which constitute one of the most abundant components of the plant microbiome. We addressed the genetic basis of host specialization in two sympatric subspecies of grass‐endophytic fungi from the Epichloë typhina complex: subsp. typhina and clarkii. The life cycle of these fungi entails unrestricted dispersal of gametes and sexual reproduction before infection of a new host, implying that the host imposes a selective barrier on viability of the progeny. We aimed to detect genes under divergent selection between subspecies, experiencing restricted gene flow due to adaptation to different hosts. Using pooled whole‐genome sequencing data, we combined FST and DXY population statistics in genome scans and detected 57 outlier genes showing strong differentiation between the two subspecies. Genomewide analyses of nucleotide diversity (π), Tajima's D and dN/dS ratios indicated that these genes have evolved under positive selection. Genes encoding secreted proteins were enriched among the genes showing evidence of positive selection, suggesting that molecular plant–fungus interactions are strong drivers of endophyte divergence. We focused on five genes encoding secreted proteins, which were further sequenced in 28 additional isolates collected across Europe to assess genetic variation in a larger sample size. Signature of positive selection in these isolates and putative identification of pathogenic function supports our findings that these genes represent strong candidates for host specialization determinants in Epichloë endophytes. Our results highlight the role of secreted proteins as key determinants of host specialization. [ABSTRACT FROM AUTHOR]

Abstract: Understanding the distribution of crossovers along chromosomes is crucial to evolutionary genomics because the crossover rate determines how strongly a genome region is influenced by natural selection on linked sites. Nevertheless, generalities in the chromosome‐scale distribution of crossovers have not been investigated formally. We fill this gap by synthesizing joint information on genetic and physical maps across 62 animal, plant and fungal species. Our quantitative analysis reveals a strong and taxonomically widespread reduction of the crossover rate in the centre of chromosomes relative to their peripheries. We demonstrate that this pattern is poorly explained by the position of the centromere, but find that the magnitude of the relative reduction in the crossover rate in chromosome centres increases with chromosome length. That is, long chromosomes often display a dramatically low crossover rate in their centre, whereas short chromosomes exhibit a relatively homogeneous crossover rate. This observation is compatible with a model in which crossover is initiated from the chromosome tips, an idea with preliminary support from mechanistic investigations of meiotic recombination. Consequently, we show that organisms achieve a higher genome‐wide crossover rate by evolving smaller chromosomes. Summarizing theory and providing empirical examples, we finally highlight that taxonomically widespread and systematic heterogeneity in crossover rate along chromosomes generates predictable broad‐scale trends in genetic diversity and population differentiation by modifying the impact of natural selection among regions within a genome. We conclude by emphasizing that chromosome‐scale heterogeneity in crossover rate should urgently be incorporated into analytical tools in evolutionary genomics, and in the interpretation of resulting patterns. [ABSTRACT FROM AUTHOR]

Abstract: Organisms typically show evidence of adaptation to features within their local environment. However, many species undergo long‐distance dispersal or migration across larger geographic regions that consist of highly heterogeneous habitats. Therefore, selection may influence adaptive genetic variation associated with landscape features at residing sites and along migration routes in migratory species. We tested for genomic adaptation to landscape features at natal spawning sites and along migration paths to the ocean of anadromous steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin. Results from multivariate ordination, gene–environment association and outlier analyses using 24,526 single nucleotide polymorphisms (SNPs) provided evidence that adaptive allele frequencies were more commonly associated with landscape features along migration paths than features at natal sites (91.8% vs. 8.2% of adaptive loci, respectively). Among the 45 landscape variables tested, migration distance to the ocean and mean annual precipitation along migration paths were significantly associated with adaptive genetic variation in three distinct genetic groups. Additionally, variables such as minimum migration water temperature and mean migration slope were significant only in inland stocks of steelhead that migrate up to 1,200 km farther than those near the coast, indicating regional differences in migratory selective pressures. This study provides novel approaches for investigating migratory corridors and some of the first evidence that environment along migration paths can lead to substantial divergent selection. Consequently, our approach to understand genetic adaptation to migration conditions can be applied to other migratory species when migration or dispersal paths are generally known. [ABSTRACT FROM AUTHOR]

Genomewide screens of genetic variation within and between populations can reveal signatures of selection implicated in adaptation and speciation. Genomic regions with low genetic diversity and elevated differentiation reflective of locally reduced effective population sizes ( Ne) are candidates for barrier loci contributing to population divergence. Yet, such candidate genomic regions need not arise as a result of selection promoting adaptation or advancing reproductive isolation. Linked selection unrelated to lineage-specific adaptation or population divergence can generate comparable signatures. It is challenging to distinguish between these processes, particularly when diverging populations share ancestral genetic variation. In this study, we took a comparative approach using population assemblages from distant clades assessing genomic parallelism of variation in Ne. Utilizing population-level polymorphism data from 444 resequenced genomes of three avian clades spanning 50 million years of evolution, we tested whether population genetic summary statistics reflecting genomewide variation in Ne would covary among populations within clades, and importantly, also among clades where lineage sorting has been completed. All statistics including population-scaled recombination rate (ρ), nucleotide diversity (π) and measures of genetic differentiation between populations ( FST, PBS, dxy) were significantly correlated across all phylogenetic distances. Moreover, genomic regions with elevated levels of genetic differentiation were associated with inferred pericentromeric and subtelomeric regions. The phylogenetic stability of diversity landscapes and stable association with genomic features support a role of linked selection not necessarily associated with adaptation and speciation in shaping patterns of genomewide heterogeneity in genetic diversity. [ABSTRACT FROM AUTHOR]

Recombination rate is heterogeneous across the genome of various species and so are genetic diversity and differentiation as a consequence of linked selection. However, we still lack a clear picture of the underlying mechanisms for regulating recombination. Here we estimated fine-scale population recombination rate based on the patterns of linkage disequilibrium across the genomes of multiple populations of two closely related flycatcher species ( Ficedula albicollis and F. hypoleuca). This revealed an overall conservation of the recombination landscape between these species at the scale of 200 kb, but we also identified differences in the local rate of recombination despite their recent divergence (<1 million years). Genetic diversity and differentiation were associated with recombination rate in a lineage-specific manner, indicating differences in the extent of linked selection between species. We detected 400-3,085 recombination hotspots per population. Location of hotspots was conserved between species, but the intensity of hotspot activity varied between species. Recombination hotspots were primarily associated with CpG islands ( CGIs), regardless of whether CGIs were at promoter regions or away from genes. Recombination hotspots were also associated with specific transposable elements ( TEs), but this association appears indirect due to shared preferences of the transposition machinery and the recombination machinery for accessible open chromatin regions. Our results suggest that CGIs are a major determinant of the localization of recombination hotspots, and we propose that both the distribution of TEs and fine-scale variation in recombination rate may be associated with the evolution of the epigenetic landscape. [ABSTRACT FROM AUTHOR]

Selection has a deep impact on the distribution of genetic diversity and population differentiation along the genome (the genomic landscapes of diversity and differentiation), reducing diversity and elevating differentiation not only at the sites it targets, but also at linked neutral sites. Fuelled by the high-throughput sequencing revolution, these genomic footprints of selection have been extensively exploited over the past decade with the aim to identify genomic regions involved in adaptation and speciation. However, while this research has shown that the genomic landscapes of diversity and differentiation are usually highly heterogeneous, it has also led to the increasing realization that this heterogeneity may evolve under processes other than adaptation or speciation. In particular, instead of being an effect of selective sweeps or barriers to gene flow, accentuated differentiation can evolve by any process reducing genetic diversity locally within the genome (Charlesworth, ), including purifying selection at linked sites (background selection). In particular, in genomic regions where recombination is infrequent, accentuated differentiation can evolve as a by-product of diversity reductions unrelated to adaptation or speciation (Cruickshank & Hahn, ; Nachman & Payseur, ; Noor & Bennett, ). In such genomic regions, linkage extends over physically larger genome stretches, and selection affects a particularly high number of linked neutral sites. Even though the effects of selection on linked neutral diversity (linked selection) within populations are well documented (Cutter & Payseur, ), recent observations of diversity and differentiation landscapes that are highly correlated even among independent lineages suggest that the effects of long-term linked selection may have a deeper impact on the evolution of the genomic landscapes of diversity and differentiation than previously anticipated. The study on Saxicola stonechats by Van Doren et al. () reported in the current issue of Molecular Ecology lines in with a rapidly expanding body of evidence in this direction. Correlations of genomic landscapes extending from within stonechats to comparisons with Ficedula flycatchers add to recent insights into the timescales across which the effects of linked selection persist. Absent and inverted correlations of genomic landscapes in comparisons involving an island taxon, on the other hand, provide important empirical clues about the role of demographic constraints in the evolution of the genomic landscapes of diversity and differentiation. [ABSTRACT FROM AUTHOR]

Seasonal migration is a widespread phenomenon, which is found in many different lineages of animals. This spectacular behaviour allows animals to avoid seasonally adverse environmental conditions to exploit more favourable habitats. Migration has been intensively studied in birds, which display astonishing variation in migration strategies, thus providing a powerful system for studying the ecological and evolutionary processes that shape migratory behaviour. Despite intensive research, the genetic basis of migration remains largely unknown. Here, we used state-of-the-art radio-tracking technology to characterize the migratory behaviour of a partially migratory population of European blackbirds ( Turdus merula) in southern Germany. We compared gene expression of resident and migrant individuals using high-throughput transcriptomics in blood samples. Analyses of sequence variation revealed a nonsignificant genetic structure between blackbirds differing by their migratory phenotype. We detected only four differentially expressed genes between migrants and residents, which might be associated with hyperphagia, moulting and enhanced DNA replication and transcription. The most pronounced changes in gene expression occurred between migratory birds depending on when, in relation to their date of departure, blood was collected. Overall, the differentially expressed genes detected in this analysis may play crucial roles in determining the decision to migrate, or in controlling the physiological processes required for the onset of migration. These results provide new insights into, and testable hypotheses for, the molecular mechanisms controlling the migratory phenotype and its underlying physiological mechanisms in blackbirds and other migratory bird species. [ABSTRACT FROM AUTHOR]

Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate 'circadian clock' genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans-Saharan migratory bird species, we investigated the relationships between species-level genetic variation at two candidate genes, Clock and Adcyap1, and species' traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in 'circadian clock' genotype frequencies, Clock allele size increased with breeding latitude across species. However, early- and late-migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long-distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long-distance migratory species, likely resulting from the time constraints imposed by late spring migration. [ABSTRACT FROM AUTHOR]

The annual migration of a bird can involve thousands of kilometres of nonstop flight, requiring accurately timed seasonal changes in physiology and behaviour. Understanding the molecular mechanisms controlling this endogenous programme can provide functional and evolutionary insights into the circannual biological clock and the potential of migratory species to adapt to changing environments. Under naturally timed photoperiod conditions, we maintained captive Swainson's thrushes ( Catharus ustulatus) and performed RNA sequencing ( RNA-Seq) of the ventral hypothalamus and optic chiasma to evaluate transcriptome-wide gene expression changes of individuals in migratory condition. We found that 188 genes were differentially expressed in relation to migratory state, 86% of which have not been previously linked to avian migration. Focal hub genes were identified that are candidate variables responsible for the occurrence of migration (e.g. CRABP1). Numerous genes involved in cell adhesion, proliferation and motility were differentially expressed (including RHOJ, PAK1 and TLN1), suggesting that migration-related changes are regulated by seasonal neural plasticity. [ABSTRACT FROM AUTHOR]

Transcontinental migration is a fascinating example of how animals can respond to climatic oscillation. Yet, quantitative data on fitness components are scarce, and the resulting population genetic consequences are poorly understood. Migratory divides, hybrid zones with a transition in migratory behaviour, provide a natural setting to investigate the micro-evolutionary dynamics induced by migration under sympatric conditions. Here, we studied the effects of migratory programme on survival, trait evolution and genome-wide patterns of population differentiation in a migratory divide of European barn swallows. We sampled a total of 824 individuals from both allopatric European populations wintering in central and southern Africa, respectively, along with two mixed populations from within the migratory divide. While most morphological characters varied by latitude consistent with Bergmann's rule, wing length co-varied with distance to wintering grounds. Survival data collected during a 5-year period provided strong evidence that this covariance is repeatedly generated by disruptive selection against intermediate phenotypes. Yet, selection-induced divergence did not translate into genome-wide genetic differentiation as assessed by microsatellites, mt DNA and >20 000 genome-wide SNP markers; nor did we find evidence of local genomic selection between migratory types. Among breeding populations, a single outlier locus mapped to the BUB1 gene with a role in mitotic and meiotic organization. Overall, this study provides evidence for an adaptive response to variation in migration behaviour continuously eroded by gene flow under current conditions of nonassortative mating. It supports the theoretical prediction that population differentiation is difficult to achieve under conditions of gene flow despite measurable disruptive selection. [ABSTRACT FROM AUTHOR]

Migration is essential for the reproduction and survival of many animals, yet little is understood about its underlying molecular mechanisms. We used the salmonid Oncorhynchus mykiss to gain mechanistic insight into smoltification, which is a morphological, physiological and behavioural transition undertaken by juveniles in preparation for seaward migration. O. mykiss is experimentally tractable and displays intra- and interpopulation variation in migration propensity. Migratory individuals can produce nonmigratory progeny and vice versa, indicating a high degree of phenotypic plasticity. One potential way that phenotypic plasticity might be linked to variation in migration-related life history tactics is through epigenetic regulation of gene expression. To explore this, we quantitatively measured genome-scale DNA methylation in fin tissue using reduced representation bisulphite sequencing of F2 siblings produced from a cross between steelhead (migratory) and rainbow trout (nonmigratory) lines. We identified 57 differentially methylated regions ( DMRs) between smolt and resident O. mykiss juveniles. DMRs were high in magnitude, with up to 62% differential methylation between life history types, and over half of the gene-associated DMRs were in transcriptional regulatory regions. Many of the DMRs encode proteins with activity relevant to migration-related transitions (e.g. circadian rhythm pathway, nervous system development, protein kinase activity). This study provides the first evidence of a relationship between epigenetic variation and life history divergence associated with migration-related traits in any species. [ABSTRACT FROM AUTHOR]

Natural history collections provide an immense record of biodiversity on Earth. These repositories have traditionally been used to address fundamental questions in biogeography, systematics and conservation. However, they also hold the potential for studying evolution directly. While some of the best direct observations of evolution have come from long-term field studies or from experimental studies in the laboratory, natural history collections are providing new insights into evolutionary change in natural populations. By comparing phenotypic and genotypic changes in populations through time, natural history collections provide a window into evolutionary processes. Recent studies utilizing this approach have revealed some dramatic instances of phenotypic change over short timescales in response to presumably strong selective pressures. In some instances, evolutionary change can be paired with environmental change, providing a context for potential selective forces. Moreover, in a few cases, the genetic basis of phenotypic change is well understood, allowing for insight into adaptive change at multiple levels. These kinds of studies open the door to a wide range of previously intractable questions by enabling the study of evolution through time, analogous to experimental studies in the laboratory, but amenable to a diversity of species over longer timescales in natural populations. [ABSTRACT FROM AUTHOR]

Migration is a key life history strategy for many animals and requires a suite of behavioural, morphological and physiological adaptations which together form the 'migratory syndrome'. Genetic variation has been demonstrated for many traits that make up this syndrome, but the underlying genes involved remain elusive. Recent studies investigating migration-associated genes have focussed on sampling migratory and nonmigratory populations from different geographic locations but have seldom explored phenotypic variation in a migratory trait. Here, we use a novel combination of tethered flight and next-generation sequencing to determine transcriptomic differences associated with flight activity in a globally invasive moth pest, the cotton bollworm Helicoverpa armigera. By developing a state-of-the-art phenotyping platform, we show that field-collected H. armigera display continuous variation in flight performance with individuals capable of flying up to 40 km during a single night. Comparative transcriptomics of flight phenotypes drove a gene expression analysis to reveal a suite of expressed candidate genes which are clearly related to physiological adaptations required for long-distance flight. These include genes important to the mobilization of lipids as flight fuel, the development of flight muscle structure and the regulation of hormones that influence migratory physiology. We conclude that the ability to express this complex set of pathways underlines the remarkable flexibility of facultative insect migrants to respond to deteriorating conditions in the form of migratory flight and, more broadly, the results provide novel insights into the fundamental transcriptional changes required for migration in insects and other taxa. [ABSTRACT FROM AUTHOR]