A genome-wide linkage map for the house sparrow (Passer domesticus) provides insights into the evolutionary history of the avian genome.

The house sparrow is an important model species for studying physiological, ecological and evolutionary processes in wild populations. Here, we present a medium density, genome wide linkage map for house sparrow (Passer domesticus) that has aided the assembly of the house sparrow reference genome, and that will provide an important resource for ongoing mapping of genes controlling important traits in the ecology and evolution of this species. Using a custom house sparrow 10 K iSelect Illumina SNP chip we have assigned 6,498 SNPs to 29 autosomal linkage groups, based on a mean of 430 informative meioses per SNP. The map was constructed by combining the information from linkage with that of the physical position of SNPs within scaffold sequences in an iterative process. Averaged between the sexes; the linkage map had a total length of 2,004 cM, with a longer map for females (2,240 cM) than males (1,801 cM). Additionally, recombination rates also varied along the chromosomes. Comparison of the linkage map to the reference genomes of zebra finch, collared flycatcher and chicken, showed a chromosome fusion of the two avian chromosomes 8 and 4A in house sparrow. Lastly, information from the linkage map was utilized to conduct analysis of linkage disequilibrium (LD) in eight populations with different effective population sizes (Ne ) in order to quantify the background level LD. Together, these results aid the design of future association studies, facilitate the development of new genomic tools and support the body of research that describes the evolution of the avian genome.

Variation and constraints in hybrid genome formation.

Hybridization is an important source of variation; it transfers adaptive genetic variation across species boundaries and generates new species. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve by sequencing the genomes of four island populations of the homoploid hybrid Italian sparrow Passer italiae. We report that a variety of novel and fully functional hybrid genomic combinations are likely to have arisen independently on Crete, Corsica, Sicily and Malta, with differentiation in candidate genes for beak shape and plumage colour. However, certain genomic regions are invariably inherited from the same parent species, limiting variation. These regions are over-represented on the Z chromosome and harbour candidate incompatibility loci, including DNA-repair and mitonuclear genes. These gene classes may contribute to the general reduction of introgression on sex chromosomes. This study demonstrates that hybrid genomes may vary, and identifies new candidate reproductive isolation genes.

The genomic mosaicism of hybrid speciation.

Hybridization is widespread in nature and, in some instances, can result in the formation of a new hybrid species. We investigate the genetic foundation of this poorly understood process through whole-genome analysis of the hybrid Italian sparrow and its progenitors. We find overall balanced yet heterogeneous levels of contribution from each parent species throughout the hybrid genome and identify areas of novel divergence in the hybrid species exhibiting signals consistent with balancing selection. High-divergence areas are disproportionately located on the Z chromosome and overrepresented in gene networks relating to key traits separating the focal species, which are likely involved in reproductive barriers and/or species-specific adaptations. Of special interest are genes and functional groups known to affect body patterning, beak morphology, and the immune system, which are important features of diversification and fitness. We show that a combination of mosaic parental inheritance and novel divergence within the hybrid lineage has facilitated the origin and maintenance of an avian hybrid species.

Rapid polygenic response to secondary contact in a hybrid species.

Secondary contact between closely related species can have genetic consequences. Competition for essential resources may lead to divergence in heritable traits that reduces interspecific competition leading to increased rate of genetic divergence. Conversely, hybridization and backcrossing can lead to genetic convergence. Here, we study a population of a hybrid species, the Italian sparrow (Passer italiae), before and after it came into secondary contact with one of its parent species, the Spanish sparrow (P. hispaniolensis), in 2013. We demonstrate strong consequences of interspecific competition: Italian sparrows were kept away from a popular feeding site by its parent species, resulting in poorer body condition and a significant drop in population size. Although no significant morphological change could be detected, after only 3 years of sympatry, the Italian sparrows had diverged significantly from the Spanish sparrows across a set of 81 protein-coding genes. These temporal genetic changes are mirrored by genetic divergence observed in older sympatric Italian sparrow populations within the same area of contact. Compared with microallopatric birds, sympatric ones are genetically more diverged from Spanish sparrows. Six significant outlier genes in the temporal and spatial comparison (i.e. showing the greatest displacement) have all been found to be associated with learning and neural development in other bird species.

Hybrid speciation in sparrows I: phenotypic intermediacy, genetic admixture and barriers to gene flow.

Homoploid hybrid speciation is thought to require unusual circumstances to yield reproductive isolation from the parental species, and few examples are known from nature. Here, we present genetic evidence for this mode of speciation in birds. Using Bayesian assignment analyses of 751 individuals genotyped for 14 unlinked, nuclear microsatellite loci, we show that the phenotypically intermediate Italian sparrow (Passer italiae) does not form a cluster of its own, but instead exhibits clear admixture (over its entire breeding range) between its putative parental species, the house sparrow (P. domesticus) and the Spanish sparrow (P. hispaniolensis). Further, the Italian sparrow possesses mitochondrial (mt) DNA haplotypes identical to both putative parental species (although mostly of house sparrow type), indicating a recent hybrid origin. Today, the Italian sparrow has a largely allopatric distribution on the Italian peninsula and some Mediterranean islands separated from its suggested parental species by the Alps and the Mediterranean Sea, but co-occurs with the Spanish sparrow on the Gargano peninsula in southeast Italy. No evidence of interbreeding was found in this sympatric population. However, the Italian sparrow hybridizes with the house sparrow in a sparsely populated contact zone in the Alps. Yet, the contact zone is characterized by steep clines in species-specific male plumage traits, suggesting that partial reproductive isolation may also have developed between these two taxa. Thus, geographic and reproductive barriers restrict gene flow into the nascent hybrid species. We propose that an origin of hybrid species where the hybrid lineage gets geographically isolated from its parental species, as seems to have happened in this system, might be more common in nature than previously assumed.

Hybrid speciation in sparrows II: a role for sex chromosomes?

Homoploid hybrid speciation in animals is poorly understood, mainly because of the scarcity of well-documented cases. Here, we present the results of a multilocus sequence analysis on the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and their proposed hybrid descendant, the Italian sparrow (P. italiae). The Italian sparrow is shown to be genetically intermediate between the house sparrow and Spanish sparrow, exhibiting genealogical discordance and a mosaic pattern of alleles derived from either of the putative parental species. The average variation on the Z chromosome was significantly reduced compared with autosomal variation in the putative parental species, the house sparrow and Spanish sparrow. Additionally, divergence between the two species was elevated on the Z chromosome relative to the autosomes. This pattern of variation and divergence is consistent with reduced introgression of Z-linked genes and/or a faster-Z effect (increased rate of adaptive divergence on the Z). F(ST) -outlier tests were consistent with the faster-Z hypothesis: two of five Z-linked loci (CHD1Z and PLAA) were identified as candidates for being subject to positive, divergent selection in the putative parental species. Interestingly, the two latter genes showed a mosaic pattern in the (hybrid) Italian sparrow; that is, the Italian sparrow was found to be fixed for Spanish sparrow alleles at CHD1Z and to mainly have house sparrow alleles at PLAA. Preliminary evidence presented in this study thus suggests that sex chromosomes may play a significant role in this case of homoploid hybrid speciation.