Multiple origins of melanism in two species of North American tree squirrel (Sciurus)

Helen R Mcrobie,Nancy D Moncrief,Nicholas I Mundy

doi:10.1186/s12862-019-1471-7

Helen R Mcrobie, Nancy D Moncrief + Show 1 more

Open Access

https://doi.org/10.1186/s12862-019-1471-7

Copy DOI

Abstract

BackgroundWhile our understanding of the genetic basis of convergent evolution has improved there are still many uncertainties. Here we investigate the repeated evolution of dark colouration (melanism) in eastern fox squirrels (Sciurus niger; hereafter “fox squirrels”) and eastern gray squirrels (S. carolinensis; hereafter “gray squirrels”).ResultsWe show that convergent evolution of melanism has arisen by independent genetic mechanisms in two populations of the fox squirrel. In a western population, melanism is associated with a 24 bp deletion in the melanocortin-1-receptor gene (MC1RΔ24 allele), whereas in a south-eastern population, melanism is associated with a point substitution in the agouti signalling protein gene causing a Gly121Cys mutation. The MC1R∆24 allele is also associated with melanism in gray squirrels, and, remarkably, all the MC1R∆24 haplotypes are identical in the two species. Evolutionary analyses show that the MC1R∆24 haplotype is more closely related to other MC1R haplotypes in the fox squirrel than in the gray squirrel. Modelling supports the possibility of gene flow between the two species.ConclusionsThe presence of the MC1R∆24 allele and melanism in gray squirrels is likely due to introgression from fox squirrels, although we cannot completely rule out alternative hypotheses including introgression from gray squirrels to fox squirrels, or an ancestral polymorphism. Convergent melanism in these two species of tree squirrels has evolved by at least two and probably three different evolutionary routes.

Highlights

While our understanding of the genetic basis of convergent evolution has improved there are still many uncertainties
All melanocortin-1 receptor (MC1R) haplotypes containing the 24 bp deletion are identical in the two species, and this includes gray squirrel populations introduced to British Columbia, Canada in the early 1900’s and gray squirrels introduced to Britain from North America in the late 1800’s [29]
The Melanocortin-1-receptor with a base pair deletion (MC1RΔ24) allele is nested within the alleles from fox squirrels, a minimum of 4 mutational steps away from all other common alleles in gray squirrels (Fig. 3, Additional file 1)

Summary

Introduction

While our understanding of the genetic basis of convergent evolution has improved there are still many uncertainties. The origin of adaptive genetic variation is one of the key issues in evolutionary biology. Such variation generally depends on new mutations or standing variation. Another less well understood means of adaptation is adaptive introgression where interspecific mating occurs followed by generations of backcrossing and selection for advantageous introgressed alleles. Adaptive introgression has been recognised for some time as an important source of genetic variation in plants, for example between sunflower species [1], between iris species [2], and between ragwort and groundsel [3]. There were fewer convincing examples in animals, an early case being between species of Australian fruit fly [4]. More recent examples include an allele at the K locus

Objectives

Methods

Results

Discussion

Conclusion