The red leopard (Panthera pardus) colour morph is a colour variant that occurs only in South Africa, where it is confined to the Central Bushveld bioregion. Red leopards have been spreading over the past 40 years, which raises the speculation that the prevalence of this phenotype is related to low dispersal of young individuals owing to high off-take in the region. Intensive selective hunting tends to remove large resident males from the breeding population, which gives young males the chance to mate with resident females that are more likely to be their relatives, eventually increasing the frequency of rare genetic variants. To investigate the genetic mechanisms underlying the red coat colour morph in leopards, and whether its prevalence in South Africa relates to an increase in genetic relatedness in the population, we sequenced exons of six colour coat associated genes and 20 microsatellite loci in twenty wild-type and four red leopards. The results were combined with demographic data available from our study sites. We found that red leopards own a haplotype in homozygosity identified by one non-synonymous SNP and a 1 bp deletion that causes a frameshift in the Tyrosinase Related Protein 1 (TYRP1), a gene known to be involved in the biosynthesis of melanin. Microsatellite analyses indicate clear signs of a population bottleneck and a relatedness of 0.11 among all pairwise relationships, eventually supporting our hypothesis that a rare colour morph in the wild has increased its local frequency due to low natal dispersal. This was backed by a high human-induced mortality rate (40%).

Coat colour and pattern are a distinguished feature in mammalian carnivores, shaped by climatic cycles and habitat type. It can be expressed in various ways, such as gradients, polymorphisms, and rare colour variants. Although natural selection explains much of the phenotypic variation found in the wild, genetic drift and heterozygote deficiency, as prominent in small and fragmented populations, may also affect phenotypic variability through the fixation of recessive alleles. The aim of this study was to test whether rare colour variants in the wild could relate to a deficiency of heterozygotes, resulting from habitat fragmentation and small population size. We present an overview of all rare colour variants in the order Carnivora, and compiled demographic and genetic data of the populations where they did and did not occur, to test for significant correlations. We also tested how phylogeny and body weight influenced the presence of colour variants with phylogenetic generalized linear mixed models (PGLMMs). We found 40 colour-variable species and 59 rare colour variants. In 17 variable phenotypic populations for which genetic diversity was available, the average AR was 4.18, HO = 0.59, and HE = 0.66, and FIS = 0.086. We found that variable populations displayed a significant reduction in heterozygosity and allelic richness compared to non-variable populations across species. We also found a significant negative correlation between population size and inbreeding coefficients. Therefore, it is possible that small effective size had phenotypic consequences on the extant populations. The high frequency of the rare colour variants (averaging 20%) also implies that genetic drift is locally overruling natural selection in small effective populations. As such, rare colour variants could be added to the list of phenotypic consequences of inbreeding in the wild.