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Abstract Studying how genetic variation is structured across space, and how it relates to divergence in phenotypic traits relevant to reproductive isolation, is important for our overall understanding of the speciation process. We used reduced-representation genomic data (ddRAD-seq) to examine patterns of genetic variation across the full distribution of an Andean warbler species complex (Myioborus ornatus–melanocephalus), which includes a known hybrid zone between two strikingly different plumage forms. Genetic structure largely reflects geographic variation in head plumage, some of which corresponds to major topographic barriers in the Andes. We also found evidence of isolation by distance shaping genetic patterns across the group’s broad latitudinal range. We found thatchrysopsandbairdi, two taxa with marked plumage differences that have a known hybrid zone, were characterized by low overall genetic divergence. Based on our cline analyses of both plumage and genomic hybrid indices, this hybrid zone extends for approximately 250 km, where advanced generation hybrids are likely most common. We also identified a slight difference in the centers of the plumage and genomic clines, potentially suggesting the asymmetric introgression ofchrysops-like plumage traits. By studying genetic variation in a phenotypically complex group distributed across a topographically complex area, which includes a hybrid zone, we were able to show how both geographic features and potentially sexually selected plumage traits may play a role in species formation in tropical mountains 

Abstract The search for the genetic basis of phenotypes has primarily focused on single nucleotide polymorphisms, often overlooking structural variants (SVs). SVs can significantly affect gene function, but detecting and characterizing them is challenging, even with long-read sequencing. Moreover, traditional single-reference methods can fail to capture many genetic variants. Using long reads, we generated a Capuchino Seedeater (Sporophila) pangenome, including 16 individuals from 7 species, to investigate how SVs contribute to species and coloration differences. Leveraging this pangenome, we mapped short-read data from 127 individuals, genotyped variants identified in the pangenome graph, and subsequently performed FST scans and genome-wide association studies. Species divergence primarily arises from SNPs and indels (< 50 bp) in non-coding regions of melanin-related genes, as larger SVs rarely overlap with divergence peaks. One exception was a 55 bp deletion near the OCA2 and HERC2 genes, associated with feather pheomelanin content. These findings support the hypothesis that the reshuffling of small regulatory alleles, rather than larger species-specific mutations, accelerated plumage evolution leading to prezygotic isolation in Capuchinos. 

Abstract Melanin-based plumage coloration in birds is shaped by pigment composition as well as melanosome morphology and distribution, however, the ways in which these factors together modulate observable color remain poorly understood. We investigate this relationship in the Capuchino Seedeaters (genusSporophila), whose recent, rapid radiation driven by sexual selection resulted in 12 species with diverse coloration patterns. Using scanning electron microscopy (SEM) and micro-computed tomography (µCT), combined with a novel application of Fontana-Masson stain to image melanosomes at high resolution, we characterize melanosome distribution and morphology in several variably colored plumage patches across Capuchino species. Melanosome morphologies followed patch-specific patterns that did not directly correlate with coloration: crown feather melanosomes were larger, more elongated, and had greater percent eumelanin content than those in belly, throat, or dorsum/rump patches. We also observed that dorsal patches had more total melanin than ventral ones, with pigment and coloration patterns suggesting possible signaling and photoprotective roles. More generally, we show how the patch-specific coloration of male Capuchinos is accompanied by differences in melanosome morphology and melanin composition and abundance. Our work highlights the challenges that remain in understanding how the nanoscale mechanisms of melanin-based pigmentation translate into macroscale plumage coloration. 

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. 

Abstract The Rufous-collared Sparrow (Zonotrichia capensis) shows phenotypic variation throughout its distribution. In particular, the Patagonian subspecies Z. c. australis is strikingly distinct from all other subspecies, lacking the black crown stripes that characterize the species, with a uniformly grey head and overall paler plumage. We sequenced whole genomes of 18 individuals (9 Z. c. australis and 9 from other subspecies from northern Argentina) to explore the genomic basis of these color differences and to investigate how they may have evolved. We detected a single ~465-kb divergence peak on chromosome 5 that contrasted with a background of low genomic differentiation and contains the suppression of tumorigenicity 5 (ST5) gene. ST5 regulates RAB9A, which is required for melanosome biogenesis and melanocyte pigmentation in mammals, making it a strong candidate gene for the melanic plumage polymorphism within Z. capensis. This genomic island of differentiation may have emerged because of selection acting on allopatric populations or against gene flow on populations in physical and genetic contact. Mitochondrial DNA indicated that Z. c. australis diverged from other subspecies ~400,000 years ago, suggesting a putative role of Pleistocene glaciations. Phenotypic differences are consistent with Gloger’s rule, which predicts lighter-colored individuals in colder and drier climates like that of Patagonia. 

Abstract Urbanization creates heterogeneous selective landscapes that cause the evolution of urban-rural clines in phenotypic traits. Although cities can introduce novel selection pressures, little attention has been paid to the role of selection outside the city in maintaining urban-rural clines. We integrate whole genome sequencing, demographic modeling, and complementary models of selection to test how natural selection in both urban and rural environments shapes the evolution of an urban-rural cline in coat color in eastern gray squirrels (Sciurus carolinensis). Coat color polymorphism in this species, which presents as either gray or melanic, is primarily determined by a 24-bp deletion in the melanocortin-1 receptor gene (Mc1R). Melanic squirrels are more prevalent in urban environments but rare or absent in rural forests. Whole genome sequencing and demographic modeling revealed substantially greater urban-rural divergence at Mc1R than the genomic background, suggesting urban-rural clines in melanism are maintained by selection. We applied three separate approaches leveraging demographic and genomic data to estimate the selection coefficient against Mc1R alleles in each habitat, producing a surprising, yet consistent finding: strong selection against the melanic morph in the rural environment and near neutrality in the city. Our findings demonstrate that selection outside the city can be sufficient to maintain urban-rural clines, and urban environments can maintain genetic diversity that would otherwise be lost in rural landscapes. This study provides a rare opportunity to unravel both the spatial dynamics and the selective pressures shaping trait variation in a widespread vertebrate species, highlighting the complex and sometimes protective role of urban landscapes in evolutionary processes. 

The Andean and Atlantic forests are separated by the open vegetation corridor, which acts as a geographic barrier. However, these forests experienced cycles of connection and isolation in the past, which shaped the phylogeographic patterns of their biotas. We analysed the evolutionary history of the rufous‐capped antshrikeThamnophilus ruficapillus, a species with a disjunct distribution in the Atlantic and Andean forests and thus an appropriate model to study the effect of the open vegetation corridor and the Andes on the diversification of the Neotropical avifauna. We performed a phylogenetic/phylogeographic analysis, including the five subspecies, using mitochondrial and nuclear genomic DNA, and studied their differences in vocalizations and plumage coloration. Both the mitochondrial and nuclear DNA evidenced a marked phylogeographic structure with three differentiated lineages that diverged without signs of gene flow in the Pleistocene (1.0–1.7 million years ago): one in the Atlantic Forest and two in the Andean forest. However, the two Andean lineages do not coincide with the two disjunct areas of distribution of the species in the Andes. Vocalizations were significantly different between most subspecies, but their pattern of differentiation was discordant with that of the nuclear and mitochondrial DNA. In fact, we did not find song differentiation between the subspecies of the Atlantic Forest and that of the northwestern Bolivian Andes, even though they differ genetically and belong to different lineages. Consistently, no differences were found in plumage coloration between the subspecies of the Atlantic Forest and that of the southern Andes. Our results suggest a complex evolutionary history in this species, which differentiated both due to dispersion across the open vegetation corridor, likely during a period of connection between the Andean and Atlantic forests, and the effect of the Bolivian Altiplano as a geographic barrier. In both cases, Pleistocene climatic oscillations appear to have influenced the species diversification. 

Abstract When facing challenges, vertebrates activate a hormonal stress response that can dramatically alter behaviour and physiology. Although this response can be costly, conceptual models suggest that it can also recalibrate the stress response system, priming more effective responses to future challenges. Little is known about whether this process occurs in wild animals, particularly in adulthood, and if so, how information about prior experience with stressors is encoded. One potential mechanism is hormonally mediated changes in DNA methylation. We simulated the spikes in corticosterone that accompany a stress response using non‐invasive dosing in tree swallows (Tachycineta bicolor) and monitored the phenotypic effects 1 year later. In a subset of individuals, we characterized DNA methylation using reduced representation bisulfite sequencing shortly after treatment and a year later. The year after treatment, experimental females had stronger negative feedback and initiated breeding earlier—traits that are associated with stress resilience and reproductive performance in our population—and higher baseline corticosterone. We also found that natural variation in corticosterone predicted patterns of DNA methylation. Finally, corticosterone treatment influenced methylation on short (1–2 weeks) and long (1 year) time scales; however, these changes did not have clear links to functional regulation of the stress response. Taken together, our results are consistent with corticosterone‐induced priming of future stress resilience and support DNA methylation as a potential mechanism, but more work is needed to demonstrate functional consequences. Uncovering the mechanisms linking experience with the response to future challenges has implications for understanding the drivers of stress resilience. 

The genetic identification of evolutionary significant units and information on their connectivity can be used to design effective management and conservation plans for species of concern. Despite having high dispersal capacity, several seabird species show population structure due to both abiotic and biotic barriers to gene flow. The Kelp Gull is the most abundant species of gull in the southern hemisphere. In Argentina it reproduces in both marine and freshwater environments, with more than 100,000 breeding pairs following a metapopulation dynamic across 140 colonies in the Atlantic coast of Patagonia. However, little is known about the demography and connectivity of inland populations. We aim to provide information on the connectivity of the largest freshwater colonies (those from Nahuel Huapi Lake) with the closest Pacific and Atlantic populations to evaluate if these freshwater colonies are receiving immigrants from the larger coastal populations. We sampled three geographic regions (Nahuel Huapi Lake and the Atlantic and Pacific coasts) and employed a reduced-representation genomic approach to genotype individuals for single-nucleotide polymorphisms (SNPs). Using clustering and phylogenetic analyses we found three genetic groups, each corresponding to one of our sampled regions. Individuals from marine environments are more closely related to each other than to those from Nahuel Huapi Lake, indicating that the latter population constitutes the first freshwater Kelp Gull colony to be identified as an evolutionary significant unit in Patagonia. 

Abstract Incomplete speciation can be leveraged to associate phenotypes with genotypes, thus providing insights into the traits relevant to the reproductive isolation of diverging taxa. We investigate the genetic underpinnings of the phenotypic differences between Sporophila plumbea and Sporophila beltoni. Sporophila beltoni has only recently been described based, most notably, based on differences in bill coloration (yellow vs. black in S. plumbea). Both species are indistinguishable through mtDNA or reduced-representation genomic data, and even whole-genome sequencing revealed low genetic differentiation. Demographic reconstructions attribute this genetic homogeneity to gene flow, despite divergence in the order of millions of generations. We found a narrow hybrid zone in southern Brazil where genetically, yet not phenotypically, admixed individuals appear to be prevalent. Despite the overall low genetic differentiation, we identified 3 narrow peaks along the genome with highly differentiated SNPs. These regions harbor 6 genes, one of which is involved in pigmentation (EDN3) and is a candidate for controlling bill color. Within the outlier peaks, we found signatures of resistance to gene flow, as expected for islands of speciation. Our study shows how genes related to coloration traits are likely involved in generating prezygotic isolation and establishing species boundaries early in speciation.