Introduction
Phenotypic variation occurs throughout the animal kingdom, and has been widely used to investigate evolutionary processes such as balancing selection and sympatric speciation (McLean & Stuart‐Fox, 2014). Coat colour and pattern, a type of phenotypic variation, have been of particular interest to evolutionary biologists due to their traceability in the wild (McKinnon & Pierotti, 2010). They are a prominent feature in mammalian carnivores, shaped by environmental factors such as past climatic cycles and habitat type (Eizirik et al., 2010). Coat colour variation can be expressed in various ways, such as gradients, polymorphisms, and rare colour variants (Figure 1). Colour gradients occur in many species, in which intermediate phenotypes or clinal variation occur along latitudal gradients in response to changing vegetation types (Taylor et al., 1990; McLean & Stuart‐Fox, 2014). A famous example of ecogeographical habitat matching is the Gloger’s rule, which describes how variation in coloration relates to climatic gradients, in which animals are more pigmented towards the equator (Caro, 2005; Delhey, 2017). It has been illustrated in, among many other taxa, hog-nosed skunks Conepatus leuconotus (Ferguson et al., 2022) and striped skunks Mephitis mephitis (Walker et al., 2023), which have reduced whiteness towards Central America, related to canopy cover. Furthermore, reddish variants are more common in open dry habitats, whereas grey and black variants are more often associated with wet areas and tropical forests respectively (Da Silva et al., 2016; 2017). Complex coat patterns, such as spots or rosettes, are more frequently found in arboreal carnivores living in densely forested areas, whereas those with uniform coats more often occur in open habitats (Allen et al., 2011).
When clearly distinguished coat variations are established within a species range, albeit at different frequencies, it is often referred to as colour polymorphism (Roulin, 2004). A species is considered polymorphic when individuals in a population display one or several colour variants that are genetically inherited and which expression is unrelated to the environment, age, sex or body condition (Buckley, 1987; Roulin, 2004). Occasional rare colour variants, that tend to be restricted to one population, are commonly not yet considered polymorphism at the species level. In the wild, rare colour variants are normally lost through fixation unless they are maintained through a rare-morph advantage or heterozygote advantage in stable populations (Gray & McKinnon, 2007). They may become abundant in populations if they have a selective benefit, such as for thermoregulation, sexual signalling, warning, or camouflage (Caro & Mallarino, 2020). Colour polymorphism may also face disruptive selection in different microhabitats, due to which spatial or temporal niche segregation can be observed in the same area (Nijhawan et al., 2019; Graipel et al., 2014; Da Silva et al., 2017). As such, new traits may allow populations to occupy new niches and facilitate range expansion (Forsman et al., 2008). Colour morphs could also be subjected to strong sexual selection, which can lead to assortative mating (Pryke & Griffith, 2007; Wellenreuther et al., 2014). Over time, this may lead to a speciation event, which implies that colour polymorphic species may represent incomplete speciation (Ford, 1945). In bird species, it was illustrated that colour polymorphic species speciate more rapidly and give rise to monomorphic daughter species (Hugall & Stuart-Fox, 2012).
Although natural selection, which may vary within a species’ geographic range, explains much of the phenotypic variation found in the wild (Da Silva et al., 2016), genetic drift and heterozygote deficiency, as prominent in small populations, may also affect phenotypic variability through the fixation of recessive alleles (Eizirik et al., 2010). It has been suggested that recent changes in coat colour or pattern may have resulted from population bottlenecks, caused by habitat fragmentation and human-induced mortality (Kubala et al., 2020). Habitat fragmentation and human-induced mortality reduce the effective size of animal populations and increases spatial isolation, which can lead to the erosion of genetic variation (Templeton et al., 1990). Specifically, inbreeding and genetic drift could result in reduced heterozygosity and allelic richness in isolated populations, which may increase the expression of rare alleles (Reed & Frankham, 2003). In other contexts, phenotypic change in small and isolated populations has already been confirmed, such as fluctuating asymmetry in brown bears Ursus arctos (Loy et al., 2021) and bone deformities in wolves Canis lupus (Räikkönen et al., 2009). It is therefore possible that the occurrence of rare colour variants may also relate to small effective population sizes. Indeed, there is some evidence that genetic drift has increased the occurrence of rare colour variants in wild carnivores, such as black tigers Panthera tigris(Sagar et al., 2021) and red leopards P. pardus (Tensen et al., 2022). At least in these cases, it is possible that small effective size had phenotypic consequences on the extant populations.
The prerequisite for colour polymorphism is genetic variation through point mutations, or base pair deletions and duplications, which can evolve in allopatry or sympatry, and through hybridization (Roulin, 2004). As illustrated in the Figure 1, many different loci and genotypes can underlie colour variants (Lyons et al., 2005a), and they can be inherited via dominant or recessive genes (Anderson et al., 2009). Important pathways involved with colour variation are pigment-type switching genes such as in the Melanocortin 1 receptor (MC1R) and Agouti signalling protein (ASIP) (Kaelin & Barsh, 2013). Typically, associated mutations are recessive and need to occur in homozygosity to affect the phenotype (Schneider et al., 2012). Due to recessive inheritance, increased frequencies of colour variants in captive-bred animals are normally achieved by establishing some level of inbreeding, increasing the level of homozygosity (Cieslak et al., 2011). For instance, many domestic cat breeds have originated from selecting missense point mutations with an autosomal recessive mode of inheritance in the tyrosinase (TYR) and tyrosinase-related protein 1 (TYRP1) (Schmidt-Küntzel et al., 2005), which is related to the albinism pathway (Lyons et al., 2005b). Therefore, rare colour variants in the wild may also be associated with the expression of recessive alleles in small and fragmented populations.
The aim of our study was to test whether colour variants in carnivores species could relate to a deficiency of heterozygotes in the wild. Although potential selective drivers cannot be ruled out, we consider that the occurrence and frequency of rare colour variants are likely associated with the increased expression of recessive alleles in small and fragmented populations. Specifically, we test the following hypotheses: (i) populations in which rare colour variants occur have a lower allelic richness and higher heterozygote deficiency than populations in which they are absent, (ii) rare colour variants occur more frequently in areas that suffer from habitat fragmentation, and (iii) rare colour variants occur more frequently in small populations. We tested these hypotheses on mammalian carnivores, because they are particularly rich in coat colour and patterns (Eizirik & Trindade, 2021). Furthermore, carnivores are vulnerable to anthropogenic habitat loss, due to their large area and food requirements, and low population densities and reproductive rates, which particularly holds true for large carnivores (Ripple et al., 2014). We here present an overview of all rare colour variants in the order Carnivora that have been reported in the wild, and compile data on genetic processes underlying these natural occurrences. By this means, we hope to gain more insights into the relationship between phenotypic variation in the wild and their underlying causes in small and fragmented populations.