Evolution of dark colour in toucans (Ramphastidae): a case of molecular adaptation?

Abstract

In the last decades, researchers have been able to determine the molecular basis of some phenotypes, to test for evidence of natural selection upon them, and to demonstrate that the same genes or genetic pathways can be associated with convergent traits. Colour traits are often subject to natural selection because even small changes in these traits can have a large effect on fitness via camouflage, sexual selection or other mechanisms. The melanocortin-1 receptor locus (MC1R) is frequently associated with intraspecific coat colour variation in vertebrates, but it has been far harder to demonstrate that this locus is involved in adaptive interspecific colour differences. Here, we investigate the contribution of the MC1R gene to the colour diversity found in toucans (Ramphastidae). We found divergent selection on MC1R in the clade represented by the genus Ramphastos and that this coincided with the evolution of darker plumage in members of this genus. Using phylogenetically corrected correlations, we show significant and specific relationships between the rate of nonsynonymous change in MC1R (dN) and plumage darkness across Ramphastidae, and also between the rate of functionally significant amino acid changes in MC1R and plumage darkness. Furthermore, three of the seven amino acid changes in MC1R that occurred in the ancestral Ramphastos branch are associated with melanism in other birds. Taken together, our results suggest that the dark colour of Ramphastos toucans was related to nonsynonymous substitutions in MC1R that may have been subject to positive selection or to a relaxation of selective pressure. These results also demonstrate a quantitative relationship between gene and phenotype evolution, representing an example of how MC1R molecular evolution may affect macroevolution of plumage phenotypes.

Widespread introgression of mountain hare genes into Fennoscandian brown hare populations

“…While it is likely that mtDNA introgression and preservation can be explained by demography [ 29 ], it is plausible that brown hare could also obtain locally adapted alleles from the resident mountain hares, which are expected to represent only a tiny fraction of the total genome. A limitation of transcriptome studies is that they provide expression data and transcript genotypes only from the sampled tissue, such as kidney or liver, and might not be able to capture genes influencing traits such as coat color variation [ 55 , 56 ], muscle metabolism [ 57 ], diet specialization [ 58 ] and immunity [ 59 ]. At present, comprehensive surveys of this type of adaptive variation in species with unknown genomes are generally not possible.…”

Detecting subtle variation in two cryptic primate families (tarsiidae and lorisidae) through morphology and genetics

“…Although the eumelanin/dark phenotype is generally considered ancestral, and several past studies have found significant amino acid changes associated with organisms presenting a pheomelanin phenotype (Valverde et al, 1995;Theron et al, 2001;Mundy & Kelly, 2003;Nasti & Timares, 2015), some studies have found significant amino acid substitutions associated with darker phenotypes too. In a study on toucans (family: Ramphastidae), Corso et al, (2016) (Nachman et al, 2003;Nunes et al, 2011;Janssen & Mundy, 2013), instead of just one or two which is seen with lighter phenotypes (Rana et al, 1999;Theron et al, 2001;Mundy & Kelly, 2003;Rosenblum et al, 2004;. It could be that the maintenance or evolution of a darker phenotype requires or allows more nonsynonymous mutations, which is what we found with the darker pottos.…”

“…It could be that the maintenance or evolution of a darker phenotype requires or allows more nonsynonymous mutations, which is what we found with the darker pottos. Another interesting finding, which correlates with the many Mc1r variation studies on bird plumage, is that the more monochromatic taxon of interest (pottos) had more Mc1r amino acid changes than the more patterned taxon (Lorisinae) (Theron et al, 2001;Mundy, 2005;Pointer & Mundy, 2011;Bourgeois et al, 2012;Corso et al, 2016). Such a finding suggests that other pigment inducing genes may be responsible for the striking coat variations found in Lorisinae.…”

“…This preference for olfactory signaling might be a useful explanation for their subdued coat color and patterns, but more research is needed to confirm such a hypothesis. Another explanation for the selection of a dark phenotype is protection from overexposure to UV radiation, which is particularly true in humans, and species that live in open areas or on the edge of forests (Valverde et al, 1995;Jablonski, 2012;Nasti & Timares, 2015;Corso et al, 2016). To our knowledge, pottos prefer dense vegetation and are nocturnal, so the effects of UV exposure would be minimal Pimley et al, 2005); in fact, as stated previously, we expect they would evolve a phenotype to help in getting more UV exposure to increase vitamin D synthesis.…”

“…A clade model analysis is used to compare/contrast a selected clade and compare it to the other clades based on known nonsynonymous changes. Branch model analyses are similarly used to select a particular branch that leads from a clade of interest to the other clades in order to infer nonsynonymous changes (Yang, 2007;Corso et al, 2016). So far, no study has investigated possible nonsynonymous changes within Lorisidae, therefore a clade or branch model seemed inappropriate for our study.…”