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Genome Study Points to Color-based Assortative Mating Effect on Crow Speciation

NEW YORK (GenomeWeb) – A genome sequencing study focused on two crow species with very different coloring patterns suggests assortative mating — including a preference for mates with like-colored plumage — can contribute to speciation.

"It could really be mostly or only this assortative mating by color that keeps the [two species] phenotypically separated," Uppsala University's Jelmer Poelstra told GenomeWeb Daily News. "As far as we know, there don't seem to be any environmental differences between the areas they inhabit."

Poelstra is co-first author on a study published online today in Science, in which he and colleagues from Sweden, Germany, and Spain described efforts to look at speciation in all-black carrion crows, Corvus (corone) corone, and gray-coated hooded crows, C. (corone) cornix, using a combination of reference genome sequencing, population resequencing, and gene expression analyses.

The hooded and carrion crows have dramatically different appearances, they explained, but are prone to mixing with one another in certain hybrid zones, including the European site tested. Indeed, findings from the study pointed to widespread introgression and gene flow between the species.

When sequence divergence did occur, it mainly fell on small, isolated genomic islands, including a region containing pigmentation, visual perception, and hormone-related genes with species-specific expression, highlighting the importance of color differences between the two.

Prior studies suggest the ancestors of C. corone and C. cornix crows became physically isolated from one another during glaciation events, the researchers noted. Despite being reintroduced and mixing after range expansions that put them in contact in a certain hybrid zone — including one running from northern to southern Europe — the hooded and carrion crows have maintained very different color patterns.

Consequently, Poelstra explained, the birds have become an intriguing model for those studying speciation. For the current paper, he and his colleagues applied genomic approaches to study the basis of this speciation further, exploring the notion that color preferences during mating might contribute to this process in the birds.

"Evidence for color-assortative mating and the independent recurrence of pied plumage phenotypes in the otherwise all-black genus Corvus has prompted the hypothesis that this color polymorphism is promoting speciation," they wrote.

To explore that possibility, the researchers started by putting together high-quality reference genome for the hooded crow species C. cornix. The 16.4-million-base assembly — covered to an average depth of 152-fold — contained nearly 20,800 predicted protein-coding genes.

The team also resequenced the genomes of 60 hooded or carrion crows at average depths of between 7.1- and 28.6-fold apiece, identifying more than 5.27 million SNPs shared between the two species and more than 8.4 million SNPs in total.

When they looked at relationships between the birds, which came from carrion crow populations in Spain and Germany and hooded crow populations in Poland and Sweden, the researchers saw extensive genetic similarities between birds from both species.

Those similarities were particularly pronounced between the two hooded crow populations and carrion crows sampled from a German population near the hybrid zone. The latter group showed closer genetic ties to the hooded crows from the other species than to more similar looking Spanish carrion crows.

When species-specific expression differences did appear, they tended to affect plumage-related genes from pigmentation pathways. For instance, the researchers saw a dip in expression of 19 genes from a melanogen pigment-producing pathway in growing feathers from hooded crow torsos.

They also detected differential expression of genes from vision and hormone-related pathways, consistent with previously described visual preference and behavioral differences between the birds.

When divergence between the two species occurred, it tended to fall in small and isolated stretches. For example, the team described a key differentiated region of just 1.95 million bases of sequences that contained all but one of 82 fixed SNP found differences between hooded and carrion crows.

The same region contained sequences coding for melanogenesis pathway players, including some of those under-expressed in the gray-patterned C. cornix crow.

Together, the team's findings hint that distinctive physical features are maintained in hooded and carrion crow species despite gene flow across all but a fraction of the genome.

"Armed with this new very detailed genetic information, it is clear that none of the currently formulated species concepts fully apply to these two crow taxa," Peter de Knijff, a human genetics researcher at Leiden University, wrote in an accompanying perspectives article.

"Put simply, apart from the few carrion crow type 'speciation islands,' German carrion crows could be considered to represent hooded crows with a black (carrion crow) phenotype," he added.

Along with additional research on hormone regulation differences in the hooded and carrion crows, Poelstra and his colleagues are gearing up to do more extensive genetic studies of crows within hybrid zones in Europe and beyond to get a better sense of the genes involved in maintaining color pattern differences.