No abstract

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d xy and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.[Supplemental material is available for this article.]Uncovering the genetic architecture of reproductive isolation and its evolutionary history are central tasks in evolutionary biology. The identification of genome regions that are highly differentiated between closely related species, and thereby constitute candidate regions involved in reproductive isolation, has recently been a major focus of speciation genetic research. Studies from a broad taxonomic range, involving organisms as diverse as plants (Renaut et al.

Hybridization in natural populations is strongly selected against when hybrid offspring have reduced fitness. Here we show that, paradoxically, pairing with another species may offer the best fitness return for an individual, despite reduced fitness of hybrid offspring. Two mechanisms reduce the costs to female collared flycatchers of pairing with male pied flycatchers. A large proportion of young are sired by conspecific male collared flycatchers through extra-pair copulations, and there is a bias in favour of male offspring (which, unlike females, are fertile) within hybrid pairs. In combination with temporal variation in breeding success, these cost-reducing mechanisms yield quantitative predictions about when female collared flycatchers should accept a male pied flycatcher as a mate; empirical data agree with these predictions. Apparent hybridization may thus represent adaptive mate choice under some circumstances.

Speciation is the combination of evolutionary processes that leads to the reproductive isolation of different populations. We investigate the significance of sex-chromosome evolution on the development of post- and prezygotic isolation in two naturally hybridizing Ficedula flycatcher species. Applying a tag-array-based mini-sequencing assay to genotype single nucleotide polymorphisms (SNPs) and interspecific substitutions, we demonstrate rather extensive hybridization and backcrossing in sympatry. However, gene flow across the partial postzygotic barrier (introgression) is almost exclusively restricted to autosomal loci, suggesting strong selection against introgression of sex-linked genes. In addition to this partial postzygotic barrier, character displacement of male plumage characteristics has previously been shown to reinforce prezygotic isolation in these birds. We show that male plumage traits involved in reinforcing prezygotic isolation are sex linked. These results suggest a major role of sex-chromosome evolution in mediating post- and prezygotic barriers to gene flow and point to a causal link in the development of the two forms of reproductive isolation.

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.

Interbreeding between species (hybridization) typically produces unfit offspring. Reduced hybridization should therefore be favored by natural selection. However, this is difficult to accomplish because hybridization also sets the stage for genetic recombination to dissociate species-specific traits from the preferences for them. Here we show that this association is maintained by physical linkage (on the same chromosome) in two hybridizing Ficedula flycatchers. By analyzing the mating patterns of female hybrids and cross-fostered offspring, we demonstrate that species recognition is inherited on the Z chromosome, which is also the known location of species-specific male plumage traits and genes causing low hybrid fitness. Limited recombination on the Z chromosome maintains associations of Z-linked genes despite hybridization, suggesting that the sex chromosomes may be a hotspot for adaptive speciation.

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.

Genomic mosaicism and novel divergence have facilitated the creation and maintenance of a hybrid species, the Italian sparrow.