Convergence in pigmentation at multiple levels: mutations, genes and function

Abstract

Convergence-the independent evolution of the same trait by two or more taxa-has long been of interest to evolutionary biologists, but only recently has the molecular basis of phenotypic convergence been identified. Here, we highlight studies of rapid evolution of cryptic coloration in vertebrates to demonstrate that phenotypic convergence can occur at multiple levels: mutations, genes and gene function. We first show that different genes can be responsible for convergent phenotypes even among closely related populations, for example, in the pale beach mice inhabiting Florida's Gulf and Atlantic coasts. By contrast, the exact same mutation can create similar phenotypes in distantly related species such as mice and mammoths. Next, we show that different mutations in the same gene need not be functionally equivalent to produce similar phenotypes. For example, separate mutations produce divergent protein function but convergent pale coloration in two lizard species. Similarly, mutations that alter the expression of a gene in different ways can, nevertheless, result in similar phenotypes, as demonstrated by sister species of deer mice. Together these studies underscore the importance of identifying not only the genes, but also the precise mutations and their effects on protein function, that contribute to adaptation and highlight how convergence can occur at different genetic levels.

Key questions in the genetics and genomics of eco-evolutionary dynamics

“…Importantly, parallelism even at the level of the gene is not universal even in the above cases: for instance, some freshwater stickleback populations show lateral plate reduction without variation in EDA (Leinonen et al, 2012;Lucek et al, 2012). Similarly diverse results are common in other organisms, with a well-described example being the evolution of color in animals (review: Manceau et al 2010).…”

“…At one extreme, adaptation by independent populations to similar environments could be driven by the same frequency changes in the same alleles (and nucleotides) at the same loci, with the relevant alleles at each locus having arisen only once (that is, identical by descent). Moving away from this extreme, the same allele might have had multiple origins, the alleles might be different but have similar effects, the alleles might be different and have different effects, and different genes might be involved in the different populations (Arendt and Reznick, 2008;Manceau et al, 2010;Linnen et al, 2013).…”

Islands as model systems in ecology and evolution: prospects fifty years after MacArthur‐Wilson

“…Accordingly, for example, it appears that 150 species of diving beetle are the product of a single colonisation event followed by speciation within the island of New Guinea (Balke et al 2007), and 1000 species of picture-winged Drosophila are the product of speciation within the Hawaiian archipelago (O'Grady et al 2011). Islands have illustrated that the factors that interact to provide conditions necessary for in situ speciation include isolation (Manceau et al 2010), age (Gillespie & Baldwin 2010) and area (Losos & Schluter 2000;Kisel & Barraclough 2010) of the region concerned, and variables often associated with area, such as topographic complexity and elevation (Whittaker et al 2008). Table 1 Under-explored or in need of revisiting: prospects for using islands to advance understanding in ecology and evolution in general.…”

On the unfounded enthusiasm for soft selective sweeps

“…Cryptic colouration has also been a fruitful area, with specific mutations in the Mc1r and Aguoti gene regions having been described as the underlying cause of adaptation for crypsis in mice of the Arizona/New Mexico lava flows 46 , Nebraska Sand Hills 23 and the Atlantic coast 47 , as well as in organisms ranging from the Siberian mammoth 48 to multiple species of lizards on the White Sands of New Mexico 49,50 (and see review ref. 51 for further examples).…”