Abstract
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.
Highlights
Hybridization between divergent populations has diverse impacts on evolution [1,2,3], including the rapid formation of hybrid species [1,2,3,4,5,6]
We suggest that speciation in this system may have been driven by dissociation of the sex (Z) chromosome into blocks of different parent speciesspecific genes, which have shifted alongside mitochondrial genes to form reproductive barriers where the hybrid meets each of its parent species
We found evidence for on-going but restricted gene exchange between Italian sparrows and house sparrows in the contact zone in the Alps (Figure S1), though no evidence for gene exchange between Italian and Spanish sparrows in the sympatric zone in southeast Italy
Summary
Hybridization between divergent populations has diverse impacts on evolution [1,2,3], including the rapid formation of hybrid species [1,2,3,4,5,6]. Homoploid hybrid speciation (HHS) is the process through which hybridization between two taxa results in a third, novel taxon that remains distinct by means of reproductive barriers against both parent taxa, without a change in number of chromosome sets. This mode of speciation is thought to be rare in nature as hybridization must be initiated by gene exchange between two taxa, but this gene exchange subsequently reduces the likelihood of hybrid speciation occurring. Whereas divergent selection on reproductive traits is expected to be heavily involved in non-hybrid speciation, increasing the influence of sex chromosomes, transgressive ecological adaptations are more likely to be autosomal and evolve under stabilizing selection in parents [8,11,12,13]. This promotes divergence on autosomes [12], and leads to a Author Summary
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