The genetic basis of adaptive melanism in pocket mice

Abstract

Identifying the genes underlying adaptation is a major challenge in evolutionary biology. Here, we describe the molecular changes underlying adaptive coat color variation in a natural population of rock pocket mice, Chaetodipus intermedius. Rock pocket mice are generally light-colored and live on light-colored rocks. However, populations of dark (melanic) mice are found on dark lava, and this concealing coloration provides protection from avian and mammalian predators. We conducted association studies by using markers in candidate pigmentation genes and discovered four mutations in the melanocortin-1-receptor gene, Mc1r, that seem to be responsible for adaptive melanism in one population of lava-dwelling pocket mice. Interestingly, another melanic population of these mice on a different lava flow shows no association with Mc1r mutations, indicating that adaptive dark color has evolved independently in this species through changes at different genes.

Figure 1

(A) Collecting localities, substrate color, and mouse color. Sample sizes at each site are given. Pie charts indicate the proportion of light and dark mice at each site. Rectangles indicate the substrate color at each site. Mice from Pinacate and Armendaris were sampled on dark lava and also on light rock adjacent to the lava, whereas mice from Avra Valley and Portal were sampled only on light rock. (B) Light and dark C. intermedius from the Pinacate locality on light and dark rocks.

Figure 2

Phylogeny of combined mitochondrial COIII and ND3 sequences of the 29 C. intermedius from the Pinacate site. Chaetodipus penicillatus and Chaetodipus baileyi were used as outgroups; all individuals in these species are light. Light and dark mice are indicated with open and filled circles, respectively. Unweighted parsimony analysis using paup^* resulted in a single shortest tree (length 132; consistency index 0.765). Numbers on branches indicate bootstrap values. The same topology was obtained when transversions were weighted 2 or 10 times more than transitions using parsimony. The same topology was also obtained by using the Neighbor-Joining algorithm.

Figure 3

Aligned Mc1r amino acid sequences (top four rows) and nucleotide sequences (bottom four rows) from C. intermedius light and dark alleles, C. penicillatus (Cp), and C. baileyi (Cb). Four amino acid differences that distinguish light and dark alleles are boxed.