Abstract
The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.
Highlights
The expression of exaggerated male traits, such as colorful ornaments or elaborate songs, often evolves under conflicting selective pressures [1], [2], [3]
Modeling the visual system of Poecilia parae When viewed through P. parae visual system, our models suggest significant differences in the perceived chromatic (F5,145 = 16.75, P,0.001; Figure 4a) and luminance (F5,145 = 41.62, P,0.001; Figure 4b) contrasts among the five male color morphs
Our results indicate that the perceived conspicuousness of the five P. parae male color morphs, as estimated by their color and luminance contrasts against the natural visual background and visual parameters of conspecifics, varied across sampling sites within populations
Summary
The expression of exaggerated male traits, such as colorful ornaments or elaborate songs, often evolves under conflicting selective pressures [1], [2], [3]. Females may favor males with highly elaborate traits, but predators and other natural enemies may likewise prefer to target these attractive males [4]. Under such scenarios, the tradeoff in attractiveness to females and susceptibility to predators can favor the evolution of reduced conspicuousness [2] or alternative ways of communicating only detectable to conspecifics [5], [6]. Variation in any of these two components of the signaling environment may influence the trade-off between attractiveness and susceptibility to predation, and favor the evolution of alternative signal design (e.g., color, song frequency) that correspond to the variable environment [2], [8], [9]. Several studies offer support for this hypothesis by showing that variation in the photic environment (manakins [10], [11], African cichlids [12], [13], [14], bluefin killifish [15], anoles lizards [16], pentamorphic Sulawesi fish [17]) and visual physiology (African cichlids [18], sticklebacks: [19], bluefin killifish [20], [21], guppy [22], passerine and avian predators [23], crab spider [24]) can favor the transmission of specific signals that can be used by conspecifics and/or predators, and promote the evolution and maintenance of color polymorphisms (see [25])
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