How the Leopard Hides Its Spots: ASIP Mutations and Melanism in Wild Cats

Alexsandra Schneider,Marilyn Menotti-Raymond,Warren E Johnson,Eduardo Eizirik,Gregory S Barsh,Victor A David,Stephen J O'Brien,William J Murphy

doi:10.1371/journal.pone.0050386

Abstract

The occurrence of melanism (darkening of the background coloration) is documented in 13 felid species, in some cases reaching high frequencies at the population level. Recent analyses have indicated that it arose multiple times in the Felidae, with three different species exhibiting unique mutations associated with this trait. The causative mutations in the remaining species have so far not been identified, precluding a broader assessment of the evolutionary dynamics of melanism in the Felidae. Among these, the leopard (Panthera pardus) is a particularly important target for research, given the iconic status of the ‘black panther’ and the extremely high frequency of melanism observed in some Asian populations. Another felid species from the same region, the Asian golden cat (Pardofelis temminckii), also exhibits frequent records of melanism in some areas. We have sequenced the coding region of the Agouti Signaling Protein (ASIP) gene in multiple leopard and Asian golden cat individuals, and identified distinct mutations strongly associated with melanism in each of them. The single nucleotide polymorphism (SNP) detected among the P. pardus individuals was caused by a nonsense mutation predicted to completely ablate ASIP function. A different SNP was identified in P. temminckii, causing a predicted amino acid change that should also induce loss of function. Our results reveal two additional cases of species-specific mutations implicated in melanism in the Felidae, and indicate that ASIP mutations may play an important role in naturally-occurring coloration polymorphism.

Highlights

Melanism is a remarkable polymorphic phenotype observed in multiple animal groups, whose occurrence may be influenced by differential adaptation to varying environments or to distinct interspecific interactions [1,2,3]
We show that two different variants of the Agouti Signaling Protein (ASIP) gene are implicated in melanistic phenotypes in the leopard and in the Asian golden cat (Pardofelis temminckii)
The single nucleotide polymorphism (SNP) detected among the P. pardus individuals was caused by a nonsynonymous mutation located in exon 4 (C333A) predicted to introduce a stop codon at amino acid position 111

Summary

Introduction

Melanism is a remarkable polymorphic phenotype observed in multiple animal groups, whose occurrence may be influenced by differential adaptation to varying environments or to distinct interspecific interactions [1,2,3]. No additional mutation involved in melanism has been identified in any of the remaining felid species exhibiting this trait, hampering a broader assessment of its evolutionary history and adaptive significance Such lack of knowledge is remarkable, as it extends to well-known and iconic animals such as the ‘black panther’, the melanistic form of the leopard (Panthera pardus) that is very common in some regions of southeastern Asia and often seen in zoos and museums. We show that two different variants of the ASIP gene are implicated in melanistic phenotypes in the leopard and in the Asian golden cat (Pardofelis temminckii) We discuss these findings in the context of the evolution of melanism, as well as the relative roles of ASIP and MC1R in the origin of such pigmentation variants

Materials and Methods

Methods

Results and Discussion