Complex genetic architecture of three-dimensional craniofacial shape variation in domestic pigeons

Abstract

Deciphering the genetic basis of vertebrate craniofacial variation is a longstanding biological problem with broad implications in evolution, development, and human pathology. One of the most stunning examples of craniofacial diversification is the adaptive radiation of birds, in which the beak serves essential roles in virtually every aspect of their life histories. The domestic pigeon (Columba livia) provides an exceptional opportunity to study the genetic underpinnings of craniofacial variation because of its unique balance of experimental accessibility and extraordinary phenotypic diversity within a single species. We used traditional and geometric morphometrics to quantify craniofacial variation in an F2 laboratory cross derived from the straight-beaked Pomeranian Pouter and curved-beak Scandaroon pigeon breeds. Using a combination of genome-wide quantitative trait locus scans and multi-locus modeling, we identified a set of genetic loci associated with complex shape variation in the craniofacial skeleton, including beak curvature, braincase shape, and mandible shape. Some of these loci control coordinated changes between different structures, while others explain variation in the size and shape of specific skull and jaw regions. We find that in domestic pigeons, a complex blend of both independent and coupled genetic effects underlie three-dimensional craniofacial morphology.

A ROR2 coding variant is associated with craniofacial variation in domestic pigeons

“…Similar to previous findings in domestic pigeons and wild birds, 20,24 3D beak and braincase shape are strongly integrated in the RH 3 OGO F 2 population (r-PLS = 0.923, p < 0.001; Figure S2B). Along the PC1 axis, all F 2 individuals are confined to a morphospace defined by the cross founders, but cluster closer to the RH than the OGO (Figure 2B).…”

“…Considering the deep evolutionary conservation of developmental pathways that regulate craniofacial morphogenesis, our findings raise the possibility that non-canonical Wnt signaling is modulated in other cases of avian craniofacial variation. We did not identify non-canonical Wnt pathway genes in our recent study of the genetic basis of pigeon beak elaboration, 24 suggesting that distinct genetic programs underlie reduction and exaggeration of the same tissues and structures.…”

“…This result is reminiscent of our analysis of pigeon beak curvature in a different study, in which F 2 individuals derived from a straightbeaked Pomeranian Pouter and curved-beaked Scandaroon more closely resembled the Pomeranian Pouter and never achieved the extreme craniofacial curvature of the Scandaroon. 24 Therefore, two different genetic crosses using four different pigeon breeds suggest that the most exaggerated versions of craniofacial traits require coordination of multiple genetic factors.…”

“…Linear measurement analysis For each F 2 individual and the cross founders, beak and braincase length were determined by calculating the linear distance between landmark pairs (beak: landmarks 1 and 2; braincase: landmarks 1 and 3 24 ) using the interlmkdist function from the R package geomorph v3.3.1. [61][62][63] Raw beak length measurements were fit to a linear regression model (beak length $body mass) and residuals were calculated in R v3.6.3.…”

“…Geometric morphometric analyses were performed in geomorph as described. 24 The NTsys landmark point dataset was imported with the readland.nts function. Missing landmarks were estimated using the function estimate.missing(method = ''TPS'').…”