It's not all black and white: investigating colour polymorphism in manta rays across Indo-Pacific populations

Abstract

Intraspecific colour polymorphisms have been the focus of numerous studies, yet processes affecting melanism in the marine environment remain poorly understood. Arguably, the most prominent example of melanism in marine species occurs in manta rays ( Mobula birostris and Mobula alfredi ). Here, we use long-term photo identification catalogues to document the frequency variation of melanism across Indo-Pacific manta ray populations and test for evidence of selection by predation acting on colour morph variants. We use mark–recapture modelling to compare survivorship of typical and melanistic colour morphs in three M. alfredi populations and assess the relationship between frequency variation and geographical distance . While there were large differences in melanism frequencies among populations of both species (0–40.70%), apparent survival estimates revealed no difference in survivorship between colour morphs. We found a significant association between phenotypic and geographical distance in M. birostris , but not in M. alfredi . Our results suggest that melanism is not under selection by predation in the tested M. alfredi populations, and that frequency differences across populations of both species are a consequence of neutral genetic processes . As genetic colour polymorphisms are often subjected to complex selection mechanisms, our findings only begin to elucidate the underlying evolutionary processes responsible for the maintenance and frequency variation of melanism in manta ray populations.

Genome-wide SNPs detect no evidence of genetic population structure for reef manta rays (Mobula alfredi) in southern Mozambique

“…Hosegood (2020) found significant genetic differentiation between sites in the Indian (the Maldives, Seychelles and Chagos Archipelago) and Pacific (Hawaii, Fiji and eastern Australia) Oceans (F ST = 0.110-0.288), yet did not detect evidence of genetic sub-structuring within populations in the Maldives or Hawaii. In addition, considerable variation in the frequency of melanistic individuals throughout other Indo-Pacific populations has been attributed primarily to genetic drift (Venables et al 2019). While these findings are indicative of limited gene flow across ocean basins and large geographic distances, little is known about the levels of genetic connectivity outside of these locations at medium-to-fine spatial scales, particularly along continuous coastlines.…”

High frequency of an otherwise rare phenotype in a small and isolated tiger population

“…Similipal has potentially been through recent bottlenecks due to the mass hunting and poaching of prey animals and regular forest fires ( 74 ). A few studies have invoked genetic drift as the driver of color polymorphism in natural populations, for example, in the northern leopard frog ( 14 ), manta ray ( 75 ), and candy-striped spider ( 12 ). Like these, our results suggest genetic drift is the major evolutionary force driving the frequency of pseudomelanism in Similipal.…”

Gudgeon fish with and without genetically determined countershading coexist in heterogeneous littoral environments of an ancient lake

“…However, the hypotheses about the ecological and evolutionary mechanisms of using countershading to attain crypsis remain poorly tested in wild aquatic organisms (Kelley & Merilaita, 2015;Kelley et al, 2017). Although some examples of noncountershaded coloration have been reported, the ecological drivers and evolutionary genetic basis underlying dark pigmentation remain unknown (Caro et al, 2011;Lindgren et al, 2014;Venables et al, 2019).…”

“…Thus, countershading is thought to be a more effective antipredator adaptation among aquatic prey species, where predators can be attacked from all directions, because dark dorsal pigmentation provides a good match to the dark background when the prey is viewed from above, whereas a light ventral surface would match the downwelling light from overhead when it is viewed from below. Partly for this reason, the loss of countershading is far less common in aquatic habitats than in terrestrial systems (Venables et al., 2019 ). However, the hypotheses about the ecological and evolutionary mechanisms of using countershading to attain crypsis remain poorly tested in wild aquatic organisms (Kelley & Merilaita, 2015 ; Kelley et al., 2017 ).…”

“…However, the hypotheses about the ecological and evolutionary mechanisms of using countershading to attain crypsis remain poorly tested in wild aquatic organisms (Kelley & Merilaita, 2015 ; Kelley et al., 2017 ). Although some examples of noncountershaded coloration have been reported, the ecological drivers and evolutionary genetic basis underlying dark pigmentation remain unknown (Caro et al., 2011 ; Lindgren et al., 2014 ; Venables et al., 2019 ). A productive way to address these questions including the functional aspects of such color patterns would be to examine aquatic animals that exhibit stable color polymorphism with either countershaded or melanistic morphs and are amenable to ecological and genetic analyses.…”