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House sparrows ( Passer domesticus ) are a hugely successful anthrodependent species; occurring on nearly every continent. Yet, despite their ubiquity and familiarity to humans, surprisingly little is known about their origins. We sought to investigate the evolutionary history of the house sparrow and identify the processes involved in its transition to a human-commensal niche. We used a whole genome resequencing dataset of 120 individuals from three Eurasian species, including three populations of Bactrianus sparrows, a non-commensal, divergent house sparrow lineage occurring in the Near East. Coalescent modelling supports a split between house and Bactrianus sparrow 11 Kya and an expansion in the house sparrow at 6 Kya, consistent with the spread of agriculture following the Neolithic revolution. Commensal house sparrows therefore likely moved into Europe with the spread of agriculture following this period. Using the Bactrianus sparrow as a proxy for a pre-commensal, ancestral house population, we performed a comparative genome scan to identify genes potentially involved with adaptation to an anthropogenic niche. We identified potential signatures of recent, positive selection in the genome of the commensal house sparrow that are absent in Bactrianus populations. The strongest selected region encompasses two major candidate genes; COL11A —which regulates craniofacial and skull development and AMY2A , part of the amylase gene family which has previously been linked to adaptation to high-starch diets in humans and dogs. Our work examines human-commensalism in an evolutionary framework, identifies genomic regions likely involved in rapid adaptation to this new niche and ties the evolution of this species to the development of modern human civilization.

Studies of reproductive isolation between homoploid hybrid species and their parent species have rarely been carried out. Here we investigate reproductive barriers between a recently recognized hybrid bird species, the Italian sparrow Passer italiae and its parent species, the house sparrow P. domesticus and Spanish sparrow P. hispaniolensis. Reproductive barriers can be difficult to study in hybrid species due to lack of geographical contact between taxa. However, the Italian sparrow lives parapatrically with the house sparrow and both sympatrically and parapatrically with the Spanish sparrow. Through whole-transcriptome sequencing of six individuals of each of the two parent species we identified a set of putatively parent species-diagnostic single nucleotide polymorphism (SNP) markers. After filtering for coverage, genotyping success (>97%) and multiple SNPs per gene, we retained 86 species-informative, genic, nuclear and mitochondrial SNP markers from 84 genes for analysis of 612 male individuals. We show that a disproportionately large number of sex-linked genes, as well as the mitochondria and nuclear genes with mitochondrial function, exhibit sharp clines at the boundaries between the hybrid and the parent species, suggesting a role for mito-nuclear and sex-linked incompatibilities in forming reproductive barriers. We suggest that genomic conflict via interactions between mitochondria and sex-linked genes with mitochondrial function (\"mother's curse\") at one boundary and centromeric drive at the other may best explain our findings. Hybrid speciation in the Italian sparrow may therefore be influenced by mechanisms similar to those involved in non-hybrid speciation, but with the formation of two geographically separated species boundaries instead of one. Spanish sparrow alleles at some loci have spread north to form reproductive barriers with house sparrows, while house sparrow alleles at different loci, including some on the same chromosome, have spread in the opposite direction to form barriers against Spanish sparrows.

The mechanisms that contribute to variation in lifetime reproductive success are not well understood. One possibility is that telomeres, conserved DNA sequences at chromosome ends that often shorten with age and stress exposures, may reflect differences in vital processes or influence fitness. Telomere length often predicts longevity, but longevity is only one component of fitness and little is known about how lifetime reproductive success is related to telomere dynamics in wild populations. We examined the relationships between telomere length beginning in early life, telomere loss into adulthood and lifetime reproductive success in free-living house sparrows (Passer domesticus). We found that females, but not males, with longer telomeres during early life had higher lifetime reproductive success, owing to associations with longevity and not reproduction per year or attempt. Telomeres decreased with age in both sexes, but telomere loss was not associated with lifetime reproductive success. In this species, telomeres may reflect differences in quality or condition rather than the pace of life, but only in females. Sexually discordant selection on telomeres is expected to influence the stability and maintenance of within population variation in telomere dynamics and suggests that any role telomeres play in mediating life-history trade-offs may be sex specific.

Behavioral evolution relies on genetic changes, yet few behaviors can be traced to specific genetic sequences in vertebrates. Here we provide experimental evidence showing that differentiation of a single gene has contributed to the evolution of divergent behavioral phenotypes in the white-throated sparrow, a common backyard songbird. In this species, a series of chromosomal inversions has formed a supergene that segregates with an aggressive phenotype. The supergene has captured ESR1, the gene that encodes estrogen receptor α (ERα); as a result, this gene is accumulating changes that now distinguish the supergene allele from the standard allele. Our results show that in birds of the more aggressive phenotype, ERα knockdown caused a phenotypic change to that of the less aggressive phenotype. We next showed that in a free-living population, aggression is predicted by allelic imbalance favoring the supergene allele. Finally, we identified cis-regulatory features, both genetic and epigenetic, that explain the allelic imbalance. This work provides a rare illustration of how genotypic divergence has led to behavioral phenotypic divergence in a vertebrate.

Animal culture evolves alongside genomes, and the two modes of inheritance—culture and genes—interact in myriad ways. For example, stable geographic variation in culture can act as a reproductive barrier, thereby facilitating genetic divergence between “cultural populations.” White-crowned sparrows ( Zonotrichia leucophrys ) are a well-established model species for bird song learning and cultural evolution, as they have distinct, geographically discrete, and culturally transmitted song types (i.e., song dialects). In this study, we tested the hypothesis that divergence between culturally transmitted songs drives genetic divergence within Nuttall’s white-crowned sparrows ( Z . l . nuttalli ). In accordance with sexual selection theory, we hypothesized that cultural divergence between mating signals both preceded and generated genetic divergence. We characterized the population structure and song variation in the subspecies and found two genetically differentiated populations whose boundary coincides with a major song boundary at Monterey Bay, California. We then conducted a song playback experiment that demonstrated males discriminate between songs based on their degree of divergence from their local dialect. These results support the idea that discrimination against non-local songs is driving genetic divergence between the northern and southern populations. Altogether, this study provides evidence that culturally transmitted bird songs can act as the foundation for speciation by sexual selection.

Phenotypic plasticity facilitates organismal invasion of novel environments, and the resultant phenotypic change may later be modified by genetic change, so called ‘plasticity first.’ Herein, we quantify gene expression plasticity and regulatory adaptation in a wild bird (Eurasian Tree Sparrow) from its original lowland (ancestral stage), experimentally implemented hypoxia acclimation (plastic stage), and colonized highland (colonized stage). Using a group of co-expressed genes from the cardiac and flight muscles, respectively, we demonstrate that gene expression plasticity to hypoxia tolerance is more often reversed than reinforced at the colonized stage. By correlating gene expression change with muscle phenotypes, we show that colonized tree sparrows reduce maladaptive plasticity that largely associated with decreased hypoxia tolerance. Conversely, adaptive plasticity that is congruent with increased hypoxia tolerance is often reinforced in the colonized tree sparrows. Genes displaying large levels of reinforcement or reversion plasticity (i.e. 200% of original level) show greater genetic divergence between ancestral and colonized populations. Overall, our work demonstrates that gene expression plasticity at the initial stage of high-elevation colonization can be reversed or reinforced through selection-driven adaptive modification.

From the northernmost tip of Scandinavia to the southernmost corner of Patagonia, and across six continents, house sparrows (Passer domesticus) inhabit most human-modified habitats of the globe. With over 7,000 articles published, the species has become a workhorse for not only the study of self-urbanized wildlife, but also for understanding life history and body size evolution, sexual selection and many other biological phenomena. Traditionally, house sparrows were studied for their adaptations to local biotic and climatic conditions, but more recently, the species has come to serve as a focus for studies seeking to reveal the genomic, epigenetic and physiological underpinnings of success among invasive vertebrate species. Here, we review the natural history of house sparrows, highlight what the study of these birds has meant to bioscience generally, and describe the many resources available for future work on this species.

The relationships of passerines (such as the well-studied zebra finch) with non-passerine birds is one of the great enigmas of avian phylogenetic research, because decades of extensive morphological and molecular studies yielded highly inconsistent results between and within data sets. Here we show the first application of the virtually homoplasy-free retroposon insertions to this controversy. Our study examined ~200,000 retroposon-containing loci from various avian genomes and retrieved 51 markers resolving early bird phylogeny. Among these, we obtained statistically significant evidence that parrots are the closest and falcons the second-closest relatives of passerines, together constituting the Psittacopasserae and the Eufalconimorphae, respectively. Our new and robust phylogenetic framework has substantial implications for the interpretation of various conclusions drawn from passerines as model organisms. This includes insights of relevance to human neuroscience, as vocal learning (that is, birdsong) probably evolved in the psittacopasseran ancestor, >30 million years earlier than previously assumed. Zebra finches are passerine birds, but their phylogenetic relationship with non-passerine birds remains controversial. By examining retroposon insertion loci in avian genomes, the authors reveal that parrots are the closest relatives of passerines, which may have implications for understanding the evolution of birdsong.

MHC genes play a fundamental role in immune recognition of pathogens and parasites. Therefore, females may increase offspring heterozygosity and genetic diversity by selecting males with genetically compatible or heterozygous MHC. In birds, several studies suggest that MHC genes play a role in mate choice, and recent evidence suggests that olfaction may play a role in the MHC-II discrimination. However, whether olfaction is involved in MHC-I discrimination in birds remains unknown. Previous studies indicate that house sparrow females with low allelic diversity prefer males with higher diversity in MHC-I alleles. Here, we directly explored whether female and male house sparrows ( Passer domesticus ) could estimate by scent MHC-I diversity and/or dissimilarity of potential partners. Our results show that neither females nor males exhibit a preference related to MHC-I diversity or dissimilarity of potential partners, suggesting that MHC-I is not detected through olfaction. Further studies are needed to understand the mechanisms responsible for mate discrimination based on MHC-I in birds.

In white-throated sparrows, two alternative morphs differing in plumage and behavior segregate with a large chromosomal rearrangement. As with sex chromosomes such as the mammalian Y, the rearranged version of chromosome two (ZAL2 m ) is in a near-constant state of heterozygosity, offering opportunities to investigate both degenerative and selective processes during the early evolutionary stages of ‘supergenes.’ Here, we generated, synthesized, and analyzed extensive genome-scale data to better understand the forces shaping the evolution of the ZAL2 and ZAL2 m chromosomes in this species. We found that features of ZAL2 m are consistent with substantially reduced recombination and low levels of degeneration. We also found evidence that selective sweeps took place both on ZAL2 m and its standard counterpart, ZAL2, after the rearrangement event. Signatures of positive selection were associated with allelic bias in gene expression, suggesting that antagonistic selection has operated on gene regulation. Finally, we discovered a region exhibiting long-range haplotypes inside the rearrangement on ZAL2 m . These haplotypes appear to have been maintained by balancing selection, retaining genetic diversity within the supergene. Together, our analyses illuminate mechanisms contributing to the evolution of a young chromosomal polymorphism, revealing complex selective processes acting concurrently with genetic degeneration to drive the evolution of supergenes.