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.