Experimental work on guppies suggests that variation in light between microhabitats is what makes females prefer different male signal combinations, thus explaining the evolution and persistence of colour variation in males.
Males of many animal species display conspicuous signals as part of their courtship — bright colours and enlarged fins in fishes or colours and feather plumes in birds are familiar examples1. Yet these displays cost energy and expose males to predation, so they will, on average, shorten the males' life. Charles Darwin identified this evolutionary paradox2, and evolutionary biologist Ronald Fisher developed a model to explain it3, arguing that if slight variation in a male trait that draws female attention initially coincides with variation in male vigour, this might trigger 'runaway selection'. Here, by means of a genetic correlation, both the male ornament and the female preference become exaggerated beyond the natural-selection optimum until natural selection and the benefit bestowed by sexual selection balance out. But this theory did not explain why considerable variation in male traits, which is widespread in nature4, should remain, because directional selection would be expected to deplete heritable variation5. Writing in American Naturalist, Cole and Endler6 suggest that environmentally dependent variation in signal transmission may be a contributing factor.
The most intuitive explanation for the maintenance of conspicuous variation in traits under strong sexual selection is that trade-offs between natural and sexual selection allow for alternative ways to optimize fitness. However, surprisingly, this idea has rarely been substantiated7. More-empirical support has accumulated for the hypothesis that expression of 'expensive-to-make' or 'expensive-to-have' signals depends on the heritable condition of the bearer. This theory may explain why variation persists in the face of strong selection either when many genes contribute to male condition, creating a large mutational target for sexual selection (the idea of 'genic capture')8, or when the relative costliness of different signals varies between different genotypes or environments9.
Cole and Endler propose a third mechanism, namely, that signal transmission and signal selection vary on very small spatial scales that affect individuals within a single population. The efficacy of animal and plant signals is a function of their transmission through the environment, their contrast against the environmental background and variables on the signal-receiver side10. The appearance and perception of colour signals, for instance, depend heavily on the light in the surrounding environment, and many animal populations occupy heterogeneous environments in which light conditions vary. The most effective signal design may then also vary between individuals depending on where and when they signal. Divergence in male signals between populations occupying either opposite ends of a light gradient or discrete habitats that differ in light conditions has been shown in other fishes, and this can be associated with species divergence, but these cases were also accompanied by divergence in the fishes' visual systems11,12,13. By controlling for visual-system variation, Cole and Endler were able to measure how sexual selection on male colour pattern changes as a function of changes in the environment alone.
The authors studied guppies — small fish that are classic study objects in the evolutionary ecology of mate choice and sexual selection14,15. Guppy males are incredibly variable in their coloration and patterns, with males displaying markedly different combinations of chromatic (including orange, red, green or blue) and achromatic (silver, black or white) colours. Guppy females are plain yellow–grey for camouflage, and vary in their mating preferences for different male colour combinations14.
By observing preferences for males in the same population of guppy females in water of four different colours, Cole and Endler estimated the attractiveness of alternative male patterns as a function of the environment. Rather than preferring individual colours, females exhibited preferences for groups of colours and for a different colour group in each environment. Female guppies seem to select entire colour patterns on the basis of overall visual contrast against the background. This implies that individuals or populations inhabiting different environments will be subject to sexual selection on male colour pattern in different directions, without any evolved change in female preferences.
The authors also report that the effectiveness of achromatic components of colour pattern changed much less with light environment than did that of chromatic colours. Although perhaps unsurprising, this observation allowed the authors to hypothesize that chromatic and achromatic colours evolve in qualitatively different ways, with the latter representing some form of contingency against environmental change. Species living in a range of light environments (generalists) would be more likely to evolve achromatic colours for signalling, whereas species that specialize on certain microhabitats would combine chromatic and achromatic components. In both of these groups, achromatic colour elements might function in aspects of communication that must work across multiple light environments — for example, the light differs on the breeding and feeding grounds of many fishes. Consequently, the authors predict that the evolution of chromatic and achromatic signals would show different levels of evolutionary conservation.
These are interesting ideas for how microevolutionary processes (those within a population) allow predictions to be made about macroevolutionary (between-species) patterns. Although testing such predictions in guppies may be difficult owing to the absence of macroevolutionary radiations in this lineage14, support comes from work on other fishes. In African cichlid fishes, of which there are large species radiations, chromatic colours tend to vary between closely related species, whereas arrangements of black stripes and bars are more strictly conserved16 (Fig. 1). And evolutionary diversification into many species that have different chromatic male courtship colours is associated with microhabitat specialization, whereas such diversification is not typically seen in habitat generalists.
The comparison between guppies and cichlids is interesting from yet other perspectives. Guppies are one of the few animals in which the genetic correlation between female preference and male trait, theoretically predicted by Fisher3 and by most models of sexual selection, has been demonstrated17. One would expect this co-evolution between the sexes to lead, at least sometimes, to behaviourally isolated species, but this has almost never happened in guppies. Ecological constraints14 and continued gene flow as a result of male coercion15 are two possible explanations, but implicit in the work of Cole and Endler is a third one: that the co-evolutionary mosaic between male colour and female preference is often mediated by environmental variation in light on so small a spatial scale that it facilitates individual variation within populations but no divergence between populations (Fig. 1). Guppies live in shallow waters of forest streams, where bright spots of sunlight alternate with canopy shade, which is depleted in red and blue light but rich in green and yellow. Individual guppies move about in this mosaic of light, and this facilitates the evolution of large colour variation between individuals within a population (called colour polymorphism) that is associated with individual light preferences. Cichlid populations in African lakes experience variation in light on a very different spatial scale, mediated by water depth, and these long and broad light gradients facilitate the divergence of entire populations across depths, eventually leading to speciation12. It seems that it is the relationship between the spatial scales of light heterogeneity and individual movement that determines whether sexual selection will maintain sexual-signal variation within populations or drive loss of variation within populations, divergence between populations and speciation.Footnote 1
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About this article
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