Melanism evolution in the cat family is influenced by intraspecific communication under low visibility

Abstract

Melanism in the cat family has been associated with functions including camouflage, thermoregulation and parasite resistance. Here we investigate a new hypothesis proposing that the evolution of melanism in cats has additionally been influenced by communication functions of body markings. To evaluate this hypothesis, we assembled a species-level data set of morphological (body marks: white marks on the backs of ears) and ecological (circadian activity: arrhythmic/nocturnal, and environmental preference: open/closed) characteristics that could be associated with communication via body markings, and combined these data with a dated molecular phylogeny. Next, we tested the association between melanism and communication, first by relating species’ body marks with their ecological conditions, using a Bayesian implementation of the threshold model. Second, to explore the evolution of characteristics potentially influencing melanism in cat species, we modeled their evolution relative to melanism using models of coordinated vs. independent character changes. Our results suggest that white marks are associated with intraspecific communication between individuals that have non-melanistic phenotypes, as well as towards melanistic individuals (without white marks). The absence of white marks in a melanistic individual tends to be a limiting condition for intraspecific visual communication at night, resulting in an evolutionary dilemma for these species, i.e. to be almost invisible at night, but not to communicate visually. The comparative analysis of several evolutionary models indicated more support for the evolution of melanism being coordinated with the evolution of arrhythmic activity and white marks on the backs of ears.

Natural Selection of Melanism in Costa Rican Jaguar and Oncilla: A Test of Gloger’s Rule and the Temporal Segregation Hypothesis

“…Artwork by Emma Mooring. compared with non-melanistic individuals (Graipel et al, 2014(Graipel et al, , 2019 and would also benefit from enhanced hunting success at those times of the day or night. We tested the prediction that the percentage of melanistic jaguar in our surveys would be higher than the global average because all of our cameras are situated in primary or secondary forests.…”

“…Of the 41 species of felids (Kitchener et al, 2017), 14 species exhibit a melanistic (black) coat morph that coexists with a wild-type "non-melanistic" coat pattern of visible spots, rosettes, or uniform color (Graipel et al, 2019;Schneider et al, 2012;Silva, 2017;Silva et al, 2016). The presence of alternative color morphs that coexist within a population, called coat color polymorphism, has long presented an evolutionary puzzle (Forsman et al, 2008;Graipel et al, 2014).…”

“…Although it has been proposed that melanistic coloration is adaptive under certain ecological conditions (Schneider et al, 2015;Silva, 2017), the functional advantages of melanism remain an enigma. The proposed functions of melanism include camouflage, thermoregulation, parasite resistance, and sexual selection (Graipel et al, 2019).…”

“…An additional factor is that many felids (including jaguar and oncilla) have white ear markings that function in intraspecific communication but are absent in melanistic individuals (Graipel et al., 2019). The combination of a dark coat and absence of white ear markings would confer melanistic felids with superior camouflage against visual predators and prey compared with more conspicuous non-melanistic conspecifics (Graipel et al., 2019).…”

“…An additional factor is that many felids (including jaguar and oncilla) have white ear markings that function in intraspecific communication but are absent in melanistic individuals (Graipel et al., 2019). The combination of a dark coat and absence of white ear markings would confer melanistic felids with superior camouflage against visual predators and prey compared with more conspicuous non-melanistic conspecifics (Graipel et al., 2019). It has recently been proposed that the benefit of short-range communication and the cost of greater conspicuousness in non-melanistic individuals should be balanced by the adaptive advantage of superior camouflage in melanistic individuals, which might explain the evolutionary persistence of melanistic polymorphisms by balancing selection in which each morph gains a different benefit (Graipel et al., 2019).…”