The genomic landscape underlying phenotypic integrity in the face of gene flow in crows

In this paper authors returned to the question about the role of interspecific gene flow for the evolution and species diversification. Authors studied hybrid zone between two bird classes of the all-black carrion crows (Corvus corone) and the gray-coated hooded crows (C. cornix). Their morphological hybrid zone in Europe gives the possibility to study the effects of introgression on evolution during early species divergence. Authors identified genome-wide introgression and showed the divergence in the expression levels of genes, implicated in plumage coloration in both species, and genes, involved in visual perception, that could be important for maintaining phenotypic differences and responsible for heterogeneity in introgression landscapes.

Principal results

Firstly, authors assembled a high-quality reference genome of one hooded crow male which was aligned to chicken and zebra finch genomes and, then, annotated through mRNA sequencing. Consequently, a set of 20.794 protein coding genes containing open reading frames of more than 100 amino acids was found. RNA seq data was used to validate identified in silico genes. Then, authors resequenced 60 genomes of unrelated birds from four populations of carrion and of hooded crows and found 8.44 million single-nucleotide polymorphisms (SNPs) segregated across all investigated populations. Interestingly, carrion and hooded crows shared just 5.27 million SNPs among all found. Authors also discovered substantial genome-wide gene flow across the hybrid zone. They observed that the major axes of genetic variation corresponded to hypothesized direction of special expansion out of Spain. Moreover, German carrion crows grouped more closely to both Swedish and Polish hooded populations than Spanish carrion crows (Figure 1). By using multiple tests, such as ABBA-BABA test, admixture analysis and coalescence-based parameter estimate of isolation-with migration model, authors proved extensive gene flow between hooded crows and the German carrion crows populations.
Further, mRNA sequencing analysis was performed on 19 individuals and five tissues to check gene expression divergence between species across the hybrid zone. However, authors observed low proportion (0.03% – 0.41%) of differently expressed genes across tissues in carrion and hooded crows. Most of differently expressed genes were responsible for plumage coloration and all found overexpressed genes were implicated in the melanogenesis pigmentation pathway (Figure 3). Nineteen of these 20 genes involved in melanogenesis were found underexpressed in the gray hooded crows. All differently expressed genes were related to growing feather follicles from the bird’s torso. Authors confirmed that gene expression bias was related to a broad spectrum of down-regulated genes implicated in melanogenesis pathway rather than to defect in melanin deposition due to various melanocytes density (Figure 4).
Then, authors investigated the landscape of genomic divergence through a 50-kb window-based approach which uses clustering algorithm reconstructing local genomic phylogenies without any a priori input hypothesis. They showed that only 0.28% of genome was divergent between carrion and hooded crows. Also, one 1.95-Mb genomic region located on chromosome 18 and exhibiting strong genetic differentiation between two species was found. This region had 81 of all 82 fixed sites between carrion and hooded crows and possessed 40 annotated protein coding genes. Moreover, it was characterized by marked reduced nucleotide diversity and differentiation in all populations and increased linkage disequilibrium (LD). Authors do not deny the possibility of inversion in this region. On Figure 2 authors demonstrated one region with recent, positive selection in hooded crows. This region had a lot of fixed hooded crow-specific derived variants and reduced values of Fu and Li’s D statistic (P < 0.05). Moreover, the region contained members of the voltage-gated calcium channel subunit gene (CACNG) family encoding for the transmembrane regulators of AMPA receptors. These proteins modulate activity of the microphtalmia-associated transcription factor gene MITF, a principal regulator of the melanogenesis (Figure 3C). Authors found 11 melanogenesis genes which were regulated by MITF and underexpressed in gray hooded crow feather follicles. Thus, the authors connect gene expression, color phenotypic differences and the signature of local divergent selection and postulate that a number of genes cause color divergence in crows. Further gene expression analysis revealed that regulator of G protein signaling 9 (RGS9), normally highly expressed in eye, together with members of SLC24 gene family, responsible for pigmentation, showed decreased expression levels in hooded crows.
To conclude, this paper underlines the significance of inversion for evolutionary process and role of sexual selection for phenotypic and genotypic differentiation.

Personal comment

This paper presents a great and complete work which deepens our understanding of the role of interspecific gene flow for the evolution and species diversification. However, on figure 1 authors showed the map of the European distribution of the carrion and hooded crows that does not linked to principal components PC1 and PC2. On my opinion, it should be better perform an analysis that links PCA to geographical coordinates, as, for example, Procrustes analysis (form of statistical shape analysis used to analyze the distribution of a set of shapes).

Poelstra, J., Vijay, N., Bossu, C., Lantz, H., Ryll, B., Muller, I., Baglione, V., Unneberg, P., Wikelski, M., Grabherr, M., & Wolf, J. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows Science, 344 (6190), 1410-1414 DOI: 10.1126/science.1253226

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