Noncoding regions underpin avian bill shape diversification at macroevolutionary scales

Abstract

<jats:title>Abstract</jats:title><jats:p>Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolutionary innovation linked to patterns of resource use, divergence and speciation, as a model trait. We integrate class-wide geometric-morphometric analyses with evolutionary sequence analyses of 10,322 protein coding genes as well as 229,001 genomic regions spanning 72 species. We identify 1,434 protein coding genes and 39,806 noncoding regions for which molecular rates were significantly related to rates of bill shape evolution. We show that homologs of the identified protein coding genes as well as genes in close proximity to the identified noncoding regions are involved in craniofacial embryo development in mammals. They are associated with embryonic stem cells pathways, including BMP and Wnt signalling, both of which have repeatedly been implicated in the morphological development of avian beaks. This suggests that identifying genotype-phenotype association on a genome wide scale over macroevolutionary time is feasible. While the coding and noncoding gene sets are associated with similar pathways, the actual genes are highly distinct, with significantly reduced overlap between them and bill-related phenotype associations specific to noncoding loci. Evidence for signatures of recent diversifying selection on our identified noncoding loci in Darwin finch populations further suggests that regulatory rather than coding changes are major drivers of morphological diversification over macroevolutionary times.</jats:p>

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

“…Our results are also consistent with studies of craniofacial genetics from diverse vertebrates; the prevailing model is that the genetic architecture of craniofacial variation is highly polygenic (Richmond et al . 2018; Yusuf et al . 2020).…”

“…2019, 2020)). In contrast, there are few examples of pairing geometric morphometric shape analysis with genome-wide scans to identify the genetic architecture of avian craniofacial variation (but see (Yusuf et al . 2020)).…”

Genomic signatures of isolation, hybridization, and selection during speciation of island finches

“…Moreover, theory and data have shown that divergence with gene flow is facilitated when selection for reduction of gene flow acts on a large part of the genome, rather than being dependent on selection on a few loci 14,15,42 . Such a situation is highly likely in the grosbeak-seedeater system as the traits under selection (bill size and shape, and body size) are well known to be under polygenic control 21,43,44 . This is supported by the relatively high level of unique polymorphisms in the grosbeak (Fig.…”

How to become a crab: Phenotypic constraints on a recurring body plan

“…As phylogenetic relationships among meiruans move towards resolution (Section 2), comparative methods could be used to identify genomic targets, for example. [120,121] Such goals come with the caveat that convergent evolution may be predictable at some hierarchical levels of biological organization, but not at others, for example. [8,122]…”