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.

Figure 1.

Genetic convergence at multiple levels. Similar phenotypes, serving the same ecological function, can evolve by: (a) changes in different genes; (b) the same mutation in the same gene; (c) different mutations in the same gene that have similar functional consequences and (d) different mutations in the same gene that affect gene function or expression in different ways.

Figure 2.

Light coloration in beach mice has evolved independently through changes in different genes. Map of the southeastern USA, in which circles represent collecting locales for P. polionotus: three mainland subspecies (brown), five Gulf Coast (red) and the two Atlantic Coast (blue) beach mouse subspecies. Atlantic and Gulf Coast beach mice have independently evolved lighter coloration, compared with their dark ancestor (cartoons). A mutation (Arg⁶⁵Cys) in Mc1r contributes to light coat colour in Gulf Coast subspecies, but not in Atlantic Coast subspecies. The most common amino acid at site 65 in each subspecies is shown: ancestral (Arg) and derived (Cys, highlighted in light red). The schematized tree represents the phylogenetic relationships of P. polionotus subspecies (P. maniculatus is shown as an outgroup; adapted from Steiner et al. 2009).

Figure 3.

Mutations in Mc1r change receptor signalling in some, but not all, species with light coloration. (a) Schematic of the Mc1r protein showing the position of amino acid variants in beach mice from Florida's Gulf (red) and Atlantic (blue) coasts, mammoths (red) and blanched lizards from White Sands, New Mexico (shades of green). Functional analysis of Mc1r alleles in (b) beach mice and mammoths and (c) lizards. Intracellular cyclic adenosine monophosphate (cAMP) accumulation was measured in response to increasing concentrations of the agonist alpha melanocyte-stimulating hormone (alpha MSH). For each taxon, the response curves for the dark Mc1r allele (brown), light allele (yellow) and control (black) are shown. Some mutations, but not all, cause a decrease in receptor signalling associated with lighter pigmentation (data taken from Hoekstra et al. 2006; Römpler et al. 2006; Steiner et al. 2009; Rosenblum et al. 2010).

Figure 4.

Genetic convergence and functional divergence in lizards. (a) In the Chihuahuan Desert of New Mexico, both the little striped whiptail (A. inornata) and the eastern fence lizard (S. undulatus) have a dark dorsal colour that closely matches the local soil colour. (b) Compared with their dark counterparts, a blanched phenotype has independently evolved in whiptail and fence lizards that colonized the dunes of White Sands. In both species, the derived phenotype results from an amino acid mutation in Mc1r (schematized). In the whiptail lizard, the derived mutation impairs Mc1r signalling activity (top right panel). In the fence lizard, a different mutation diminishes the efficiency of Mc1r integration into the melanocyte membrane (bottom right panel). Phenotypic convergence (blanched colour) is reflected at the genetic level (mutations in the same gene, Mc1r), but not at the functional level (mutations have different effects on protein function).

Figure 5.

Genetic convergence and functional divergence in deer mice. (a) The Agouti gene produces two transcriptional isoforms. Both contain exons 2 to 4, but they differ in the first, untranslated exons—the ventral-specific isoform contains exons 1A and 1A′, whereas the hair-cycle-specific isoform contains exons 1B and 1C. In populations of two sister species, (b) P. polionotus and (c) P. maniculatus, derived mutations in the Agouti gene result in an overall lighter coat colour, which is cryptic in novel habitat (the sand dunes of the Florida Coast or Nebraska's Sand Hills, respectively). However, Agouti mutations act through different changes in gene expression: in beach mice, changes in Agouti expression may primarily modify colour pattern, whereas in Sand Hills mice, Agouti mutations mainly modify pigment type and distribution on individual hairs (i.e. a wider phaeomelanin band). These results suggest that different isoforms might be targeted—the ventral Agouti isoform in beach mice and the hair-cycle-specific isoform in Sand Hills mice.