Convergent Evolution of Head Crests in Two Domesticated Columbids Is Associated with Different Missense Mutations inEphB2

Abstract

Head crests are important display structures in wild bird species and are also common in domesticated lineages. Many breeds of domestic rock pigeon (Columba livia) have crests of reversed occipital feathers, and this recessive trait is associated with a nonsynonymous coding mutation in the intracellular kinase domain of EphB2 (Ephrin receptor B2). The domestic ringneck dove (Streptopelia risoria) also has a recessive crested morph with reversed occipital feathers, and interspecific crosses between crested doves and pigeons produce crested offspring, suggesting a similar genetic basis for this trait in both species. We therefore investigated EphB2 as a candidate for the head crest phenotype of ringneck doves and identified a nonsynonymous coding mutation in the intracellular kinase domain that is significantly associated with the crested morph. This mutation is over 100 amino acid positions away from the crest mutation found in rock pigeons, yet both mutations are predicted to negatively affect the function of ATP-binding pocket. Furthermore, bacterial toxicity assays suggest that "crest" mutations in both species severely impact kinase activity. We conclude that head crests are associated with different mutations in the same functional domain of the same gene in two different columbid species, thereby representing striking evolutionary convergence in morphology and molecules.

Pigeonetics takes flight: Evolution, development, and genetics of intraspecific variation

“…Notably, many of the traits that vary among pigeons also vary among other avian species (Baptista et al, 2009; Price, 2002). Complementary genetic, genomic, and developmental approaches are enabling the rapid discovery of the molecular basis of astonishing variation among pigeons, thereby opening new avenues to understand the potential roles of specific genes in variation among vertebrates in general (Baptista et al, 2009; Domyan et al, 2016; Vickrey et al, 2015). The limited fecundity of females and dearth of commercial hatcheries makes obtaining material for embryonic manipluation more difficult in pigeon than in chicken, but embryos of both species develop in ovo , and we expect that gene perturbation technologies developed for chicken will be readily-transferrable to the pigeon model, as well.…”

“…2). As in domestic pigeons, crested ringneck doves have an amino acid substitution at a highly conserved residue in the catalytic site of the EPHB2 kinase domain (Vickrey et al, 2015). Both mutations produce kinase-dead versions of EPHB2, yet the amino acid substitutions found in pigeon and ringneck dove are separated by more than 100 residues and are predicted to have different effects on protein function.…”

“…Both mutations produce kinase-dead versions of EPHB2, yet the amino acid substitutions found in pigeon and ringneck dove are separated by more than 100 residues and are predicted to have different effects on protein function. The pigeon mutation is predicted to destabilize the active site by breaking a critical salt bridge, while the dove mutation likely hinders entrance of ATP into the catalytic domain (Carrera et al, 1993; Hemmer et al, 1997; Vickrey et al, 2015). Thus, different mutations in the same gene result in similar phenotypes in two columbid species that diverged over 20 million years ago (Goodwin, 1983; Pereira et al, 2007).…”

“…This situation offers a rich set of animal resources to test whether the same or different genes – and the same or different mutations in those genes – underlie this phenotypic similarity. Understanding how these similarities arise is an area of intense interest in evolutionary developmental biology and genetics (Christin et al, 2010; Hovav et al, 2008; Martin and Orgogozo, 2013; Paterson et al, 1995; Rosenblum et al, 2014; Stern, 2013; Vickrey et al, 2015). …”

Genomic determinants of epidermal appendage patterning and structure in domestic birds

“…In both domestic pigeons and ringneck doves, crest ( cr locus) is a recessive trait characterized by a regional reversal in growth polarity such that feathers grow in a cranial rather than caudal direction on the back of the head and neck (Figure 3A–B) (Levi, 1986; Shapiro et al, 2013; Vickrey et al, 2015). Examination of feather placode polarity in crested and uncrested domestic pigeon embryos suggests that disruption of epidermal polarity occurs early in development prior to feather outgrowth (Shapiro et al, 2013).…”