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Lovette, I. J.

Publications and source records attributed to Lovette, I. J..

12 recordsLinked to original sources

Seeking smarts: Male chickadees with better spatial cognition sire more extra-pair young

Across animal taxa, females commonly mate with more than one male, even in monogamous mating systems. These extra-pair (EP) copulations and resulting young may increase the fitness of the female via a variety of mechanisms. The "good genes" hypothesis suggests that socially monogamous females mate outside their pair bond to increase the fitness of their offspring via indirect genetic benefits, because extra-pair males do not provide parental care. We tested this hypothesis by quantifying extra-pair paternity in nonmigratory, food-caching mountain chickadees (Poecile gambeli). Chickadees rely on spatial cognition to recover scattered food caches and variation in spatial cognition is associated with increased survival, longer lifespan, and is heritable. However, less is known about the role of sexual selection on spatial cognitive abilities. In the current study, we found that 1. males with better spatial cognitive abilities sired more extra-pair young and produce heavier offspring in their own nests compared to their poorer performing counterparts, and 2. extra-pair males had significantly better spatial cognition than the social males they cuckolded. These results suggest that sexual selection shapes the evolution of spatial cognition in food-caching chickadees and are consistent with the good genes hypothesis, which posits that females gain indirect genetic benefits via extra-pair young.

animal behavior and cognition↗

Diversification and divergence in Myioborus warblers: insights into evolutionary relationships and plumage genetics

Genomic data can provide valuable insights into the evolutionary history of rapidly diversifying groups and the genetic basis of phenotypic differences among lineages. We used whole-genome sequencing of the warbler genus Myioborus to investigate dynamics of its recent diversification in Neotropical mountains. We found that mitochondrial and UCE phylogenies are mostly, but not fully, concordant, and we found phylogenetic support for a pattern of north-to-south and low-to-high elevation colonization in the genus. Within the ornatus-melanocephalus complex, which showed topological incongruence between our phylogenies, we found that genetic structure generally coincides with geographic variation in plumage, although three subspecies with striking plumage differences exhibit low mitochondrial divergence. The hybridizing taxa M. o. chrysops and M. m. bairdi show very shallow genomic differentiation, with marked peaks of divergence. Most of these are shared with other parulid warbler pairs, pointing to broad genomic features, like recombination rate, as the processes shaping these regions. However, other highly differentiated regions were unique to Myioborus, including one containing the gene CCDC91, which is associated with melanin-based plumage differences in several other birds. Lastly, we found higher levels of differentiation on the Z chromosome relative to autosomes, including two putative chromosomal inversions. Together, these results highlight the interplay of deep ancestral divergence, recent hybridization, and shared genomic architecture in shaping the evolution of phenotypic and genomic diversity within Myioborus.

evolutionary biology↗

Recent divergence and microgeographic genetic structure in an endangered Australian songbird: the southern black-throated finch

Anthropogenic habitat loss and climate change threaten global biodiversity. Effective conservation management requires a detailed understanding of geographic structure, genetic diversity, and demography of threatened species. The black-throated finch, Poephila cincta, is an Australian songbird with two subspecies: atropygialis and cincta. The southern subspecies, cincta, has experienced an [~]80% range contraction over the last century and is listed as endangered but genetic surveys of it are incomplete. Here, we use a combination of reduced representation and whole genome sequencing to examine genetic differentiation, spatial genetic structure, and demographic history in both forms of this species. We find that atropygialis and cincta are genetically distinct despite a history of divergence with gene flow and geographically isolated by a biogeographic barrier known as the Einasleigh Uplands. Since they last shared a common ancestor [~]400,000 years ago, the two subspecies have experienced distinct demographic trajectories: population expansion in atropygialis and population decline in cincta. We find that the two remnant population centers of cincta, from the Galilee Basin and the Townsville Coastal Plain, each represent genetically distinct lineages that last shared appreciable levels of gene flow [~]4,000 years ago. Moreover, we report striking microgeographic genetic structure from the Townsville Coastal Plain between populations <20 km apart associated with barriers to dispersal caused by anthropogenic habitat modification over the last 50 years: namely the construction of the Ross River Dam. Our findings highlight the urgent need for a conservation approach that prioritizes habitat restoration to re-establish population connectivity in the endangered southern black-throated finch.

evolutionary biology↗

Genomes of the extinct Bachman's Warbler shows high divergence and no evidence of admixture with other extant Vermivora Warblers

Bachmans Warbler (Vermivora bachmanii) - last sighted in 1988 - is one of the few North American passerines that have gone extinct. Given the extensive ongoing hybridization of its two extant congeners - the Blue-Winged Warbler (V. cyanoptera) and Golden-Winged Warbler (V. chrysoptera) - and shared patterns of plumage variation between Bachmans Warbler and hybrids between those extant species, it has been suggested that Bachmans Warbler might have also had a component of hybrid ancestry. Here, we use historic DNA (hDNA) and whole genome sequencing of Bachmans Warblers collected at the turn of the 20th century to address this possibility. We combine these data with genomes of the two extant Vermivora species to examine patterns of population differentiation, inbreeding, and gene flow. In contrast to the admixture hypothesis, the genomic evidence is consistent with V. bachmanii being a highly divergent, reproductively isolated species, with no evidence of introgression. We show that both V. bachmanii and V. chrysoptera have elevated runs of homozygosity compared to V. cyanoptera, consistent with the effects of a small effective population size or population bottlenecks in the former two species. We also found--using population branch statistic estimates of all three species--previously undocumented evidence of lineage-specific evolution in V. chrysoptera near a novel pigmentation gene candidate for warblers, CORIN, which is a known modifier of ASIP, which is in turn involved in melanic throat and mask coloration in this family of birds. Together, these genomic results also highlight how natural history collections are such invaluable repositories of information about extant and extinct species. SignificanceFew common North American passerines have gone extinct. Bachmans Warbler is, unfortunately, one that has--the last sighting was in 1988. Here we use whole genome historical DNA from museum specimens of Bachmans warblers collected at the turn of the 20th century to learn about the evolution of this species and test whether there was evidence for hybridization and gene flow between it and two extant members of the same genus which, today, hybridize extensively. We find Bachmans warbler was highly divergent with no evidence of gene flow. We also find evidence of elevated "runs of homozygosity" in both Bachmans warbler and one of the two extant Vermivora species, suggesting the effects of a small population size or population bottlenecks.

evolutionary biology↗

Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps

Numerous studies of emerging species have identified genomic "islands" of elevated differentiation against a background of relative homogeneity. The causes of these islands remain unclear, however, with some signs pointing toward "speciation genes" that locally restrict gene flow and others suggesting selective sweeps that have occurred within nascent species after speciation. Here, we examine this question through the lens of genome sequence data for five species of southern capuchino seedeaters, finch-like birds from South America that have undergone a species radiation during the last [~]50,000 generations. By applying newly developed statistical methods for ancestral recombination graph inference and machine-learning methods for the prediction of selective sweeps, we show that previously identified islands of differentiation in these birds appear to be generally associated with relatively recent, species-specific selective sweeps, most of which are predicted to be "soft" sweeps acting on standing genetic variation. Many of these sweeps coincide with genes associated with melanin-based variation in plumage, suggesting a prominent role for sexual selection. At the same time, a few loci also exhibit indications of possible selection against gene flow. These observations shed new light on the complex manner in which natural selection shapes genome sequences during speciation. Significance StatementGenome-wide scans can identify differentiated loci between species that may have promoted speciation. So-called "islands of differentiation" have generally been identified and characterized using standard population genetic summary statistics (e.g., FST and dxy), which are limited in distinguishing among possible causes of differentiation, such as selection against gene flow and selective sweeps. We introduce a powerful strategy for analyzing such islands, combining new methods for inferring the full Ancestral Recombination Graph and machine learning methods for identifying selective sweeps. We applied our methods to genomic sequences from closely related southern capuchino seedeaters (Neotropical tanagers) and found signatures of recent selective sweeps around pigmentation genes, including many "soft" sweeps that acted on standing variation.

evolutionary biology↗

Selection on a pleiotropic color gene block underpins early differentiation between two warbler species

When one species gradually splits into two, divergent selection on specific traits can cause peaks of differentiation in the genomic regions encoding those traits. Whether speciation is initiated by strong selection on a few genomic regions with large effects or by more diffused selection on many regions with small effects remains controversial. Differentiated phenotypes between differentiating lineages are commonly involved in reproductive isolation, thus their genetic underpinnings are key to the genomics architecture of speciation. When two species hybridize, recombination over multiple generations can help reveal the genetic regions responsible for the differentiated phenotypes against a genomic background that has been homogenized via backcrossing and introgression. We used admixture mapping to investigate genomic differentiation and the genetic basis of differentiated plumage features (relative melanin and carotenoid pigment) between hybridizing sister species in the early stage of speciation: Townsends (Setophaga townsendi) and Hermit warblers (S. occidentalis). We found a few narrow and dispersed divergent regions between allopatric parental populations, consistent with the divergence with gene flow model of speciation. One of the divergent peaks involves three genes known to affect pigmentation: ASIP, EIF2S2, and RALY (the ASIP-RALY gene block). After controlling for population substructure, we found that a single nucleotide polymorphism (SNP) inside the intron of RALY displays a strong pleiotropic association with cheek, crown, and breast coloration. In addition, we detect selection on the ASIP-RALY gene block, as the geographic cline of the RALY marker of this gene block has remained narrower than the plumage cline, which remained narrower than expected under neutral diffusion over two decades. Despite extensive gene flow between these species across much of the genome, the selection on ASIP-RALY gene block maintains stable genotypic and plumage difference between species allowing further differentiation to accumulate via linkage to its flanking genetic region or linkage-disequilibrium genome-wide.

evolutionary biology↗

Genome Report: De novo assembly of a high-quality reference genome for the Horned Lark (Eremophila alpestris)

The Horned Lark (Eremophila alpestris) is a species of small songbird that exhibits remarkable geographic variation in appearance and habitat across an expansive distribution. While E. alpestris and related species have been the focus of many ecological and evolutionary studies, we still lack a highly contiguous genome assembly for horned larks and related taxa (Alaudidae). Here, we present CLO_EAlp_1.0, a highly contiguous assembly for horned larks generated from blood samples of a wild, male bird captured in the Altiplano Cundiboyacense of Colombia. By combining short-insert and mate-pair libraries with the ALLPATHS-LG genome assembly pipeline, we generated a 1.04 Gb assembly comprised of 2708 contigs with an N50 of 10.58 Mb and a L50 of 29. After polishing the genome, we were able to identify 94.5% of single-copy gene orthologs from an Aves data set and 97.7% of single-copy gene orthologs from a vertebrata data set, indicating that our de novo assembly is near complete. We anticipate that this genomic resource will be useful to the broader ornithological community and those interested in studying the evolutionary history and ecological interactions of a widespread, yet understudied lineage of songbirds.

genomics↗

Environment but not geography explains genetic variation in the invasive and largely panmictic European starling in North America

Populations of invasive species that colonize and spread in novel environments may differentiate both through demographic processes and local selection. European starlings (Sturnus vulgaris) were introduced to New York in 1890 and subsequently spread throughout North America, becoming one of the most widespread and numerous bird species on the continent. Genome-wide comparisons across starling individuals and populations can identify demographic and/or selective factors that facilitated this rapid and successful expansion. We investigated patterns of genomic diversity and differentiation using reduced-representation genome sequencing (ddRADseq) of 17 winter-season starling populations. Consistent with this species high dispersal rate and rapid expansion history, we found low geographic differentiation and few FST outliers even at a continental scale. Despite starting from a founding population of approximately 180 individuals, North American starlings show only a moderate genetic bottleneck, and models suggest a dramatic increase in effective population size since introduction. In genotype-environment associations we found that [~]200 single-nucleotide polymorphisms are correlated with temperature and/or precipitation against a background of negligible genome- and range-wide divergence. Local adaptation in North American starlings may have evolved rapidly even in this wide-ranging and evolutionarily young population. This survey of genomic signatures of expansion in North American starlings is the most comprehensive to date and complements ongoing studies of world-wide local adaptation in these highly dispersive and invasive birds.

evolutionary biology↗

Selection on VPS13A linked to long-distance migratory behavior in a songbird

Animal migration demands an interconnected suite of physiological, behavioral, and neurological adaptations for individuals to successfully navigate and travel over long distances1-3. This trait complex is especially crucial for small songbirds whose migratory behaviors--like directionality and orientation--are innate4,5, rather than being learned as in many large, longer-lived birds. Identifying causal genes involved in these traits has been a central goal of migration ecology, and this endeavor has been furthered by genome-scale comparisons6. However, even the most successful studies of migration genetics have only achieved low resolution associations, identifying large chromosomal regions, across multiple haplotype blocks, that encompass hundreds of putatively causal genes7,8. Here we leverage the extreme genomic similarity among golden-winged (Vermivora chrysoptera) and blue-winged warblers (Vermivora cyanoptera)9 to identify a single gene--Vacuolar Protein Sorting 13 Homolog A (VPS13A)--that is associated with distinct differences in migration directionality to Central American (CA) versus South American (SA) wintering areas10. Moreover, we find significantly reduced sequence variation in this gene-region for SA wintering birds, and show this is the result of strong natural selection on this gene. In humans, VPS13A codes for chorein, and variants of this gene are associated with the neurodegenerative disorder chorea-acanthocytosis11. This new association provides the strongest gene-level linkage for avian migration directionality, and further interrogation of this gene will allow for a better understanding of its role in neuro-muscular processes across vertebrates.

evolutionary biology↗

Black or red: A sex-linked colour polymorphism in a songbird is maintained by balancing selection

Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. We therefore used genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We found that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-{beta} superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we found no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.

evolutionary biology↗

Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird

Information on genetic relationships among individuals is essential to many studies of the behavior and ecology of wild organisms. Parentage and relatedness assays based on large numbers of SNP loci hold substantial advantages over the microsatellite markers traditionally used for these purposes. We present a double-digest restriction site-associated DNA sequencing (ddRAD-seq) analysis pipeline that, as such, simultaneously achieves the SNP discovery and genotyping steps and which is optimized to return a statistically powerful set of SNP markers (typically 150-600 after stringent filtering) from large numbers of individuals (up to 240 per run). We explore the tradeoffs inherent in this approach through a set of experiments in a species with a complex social system, the variegated fairy-wren (Malurus lamberti), and further validate it in a phylogenetically broad set of other bird species. Through direct comparisons with a parallel dataset from a robust panel of highly variable microsatellite markers, we show that this ddRAD-seq approach results in substantially improved power to discriminate among potential relatives and considerably more precise estimates of relatedness coefficients. The pipeline is designed to be universally applicable to all bird species (and with minor modifications to many other taxa), to be cost- and time-efficient, and to be replicable across independent runs such that genotype data from different study periods can be combined and analyzed as field samples are accumulated.

animal behavior and cognition↗

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of genomic differentiation among independent lineages can provide insights into aspects of the speciation process, such as the relative importance of selection and drift in shaping genomic landscapes, the role of genomic regions of high differentiation, and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and divergence in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology, and migratory behavior, to ask whether similar genomic regions are important in the evolution of independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from 5 taxa and found that patterns of genetic diversity and divergence are highly similar among different stonechat taxa. We then asked if 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 in reproductive isolation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or facilitate local adaptation.

genomics↗