Black or grey colouration can mean life or death; choose a mate wisely

The grey wolf, Canis lupus, is an apex predator that is widely distributed across the globe in stable populations, often under conservation. Despite their title, both black and grey variants coexist; puzzling academics as to whether a mix of both holds adaptive value. The frequency of black wolves increases heading south-west across the continent of North America, and it has been hypothesised that this is caused by changing selection pressures.

In an effort to untangle the evolutionary reason for this pattern, a recent study published in Science has linked the cline in frequency of black wolves to the prevalence of a disease, canine distemper virus.

Periodic and localised outbreaks of CDV create fluctuating selective pressure, which the researchers theorise contributes to the evolution of mating strategies, and consequently the composition of colours among wolf populations. The underlying mechanism has been revealed to be the pleiotropic effects of the gene CBD103 coupling coat colour to immunocompetency, allowing resistance to be visually signalled to potential mates.

Led by Professor Tim Coulson from the University of Oxford, the study nimbly assembles a variety of data, modelling, and statistical analysis to construct a robust argument supporting their hypotheses. The magnitude of the data, vast geographical range, and time span sculpt a convincing argument.

CDV is a measles-like virus that can be fatal in juveniles and cause long term health defects in adult wolves, including seizures and blindness. Likened to COVID-19 by one of the authors, CDV can spread rapidly among large social groups of wolves; at points reaching a mortality rate of 50%. Variations in outbreaks can cause shifting selective pressure, as wolves with superior immune capacity will be more likely to survive CDV outbreaks, conferring higher relative fitness. Fitness encompasses an organism’s ability to survive and reproduce in its current spatiotemporal environment, and so is intrinsically dynamic and reliant on environmental conditions.

It was found that black coat colour was positively correlated with the presence of CDV antibodies, at the level of the individual and across entire populations. The molecular apparatus responsible is centred around the gene CBD103. In wolves, its protein interacts with the melanocortin pathway, which controls pigment-type switching. The wild type k allele permits normal epistatic interactions between the components agouti and Mc1r, resulting in a grey phenotype. The mutated K allele, a result of three nucleotides being deleted, prevents agouti from normal functioning, resulting in a black coat.

Simultaneously, the K locus also encodes a β-defensin protein involved in the immune response to respiratory diseases such as CDV. Therefore, the genotype has direct effects on the fitness of the individual, which is advertised by the colourful by-product.

The fitness consequences of the available genotypes vary in relation to the environmental content at the time. Employing data from wolves in Yellowstone National Park, the relationship between life history and coat colour was analysed. Grey females were shown to have 25% greater reproductive success than their black counterparts. However, through sampling over five CDV outbreaks, the study indicates that when CDV is prevalent, black wolves hold an advantage in their ability to survive the disease. In such circumstances, heterozygous black wolves have the highest fitness, due to a trade-off between reproductive success and immunity.

Therefore, the long term evolutionarily stable strategy, in locations where CDV outbreaks occur more than once every ten years, proves to be dissociative mating. This maximises the likelihood that offspring will be heterozygous and able to capitalise on the fitness trade off. Wolves in Yellowstone National Park do behave according to this model, resulting in stable polymorphism among the wolf population. Additionally, the study employed modelling to map historical outbreaks of CDV to the colour composition of populations and found that the most likely explanation for the number of black wolves was interbreeding between black and grey wolves. Notably, this tactic is only advantageous where CDV is prevalent; the relative frequency of black wolves in populations which do not experience CDV often is much lower.

This study holds relevance across a range of applications, spanning the conservation of wolves to broader investigations of evolution and sexual selection across the animal kingdom. In many cases, colour is an important signal of dominance and immunological robustness, which have direct implications for fitness. For example, colouration is associated with disease resistance MHC genes in birds and is used to inform mate choice.

Thus, the remarkable power of pathogens has manifested in the evolution of physiological traits and behaviour. In the case of wolves, the complex interactions between a pathogen and its host have cultivated a sophisticated system of mate choice, where a black or grey coat can be the difference between life and death.


Image: Marc-Olivier Jodoin on Unsplash

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