Research on guppies provides the most definitive evidence yet for the rare-male effect — a long-standing hypothesis to explain the perplexing maintenance of variation in traits that are subject to strong mate choice. See Letter p.108
The little fish commonly known as guppies are almost as popular among evolutionary biologists as they are among home aquarists, because they provide a tantalizing opportunity to explore how genetic variation is maintained in natural populations. The males of this species (Poecilia reticulata) present a dazzling display of colour variation, and it is known that female guppies show strong mating preferences on the basis of male colour patterns. But the maintenance of this colour variation presents an evolutionary mystery, because sexual selection for a specific form of a trait should erode variation in that trait1. The discovery2 that, in a natural setting, male guppies with rare colour patterns survive better than more common types, presumably because they are less often targeted by predators, was an important advance in explaining guppy colour diversity. Now, on page 108 of this issue, members of the same research group (Hughes et al.3) show that wild guppy males with rare traits obtain more matings and leave more offspring. Thus, it seems that the diverse coloration in this species is promoted by both natural and sexual selection.
Negative frequency-dependent selection — which in the case of sexual selection is sometimes called the rare-male effect — is a process in which the evolutionary fitness of a trait goes up as its relative abundance goes down. The literature on this effect goes back a long way and is substantial, but has at times been heavily criticized4,5. Some of the best available evidence has come from investigations of guppies in the laboratory, in which preferences for both unfamiliar and rare traits (phenotypes) have been documented6,7. But the relevance of such laboratory results to natural populations has been open to question because of a lack of studies in natural settings7,8.
Hughes and colleagues' study is noteworthy in large part because it involves naturally occurring male colour phenotypes in natural pools located along streams in Trinidad. To perturb these stream systems from a possible evolutionary equilibrium in the abundance of different colour patterns, and to enhance the power to detect negative frequency-dependent selection, the authors experimentally adjusted the frequencies of different types of males (Fig. 1). For balance, they made the same phenotypes rare in some pools and common in others. Then, to evaluate the reproductive success of the males, they undertook the daunting task of genotyping more than 1,400 offspring of pregnant females collected from the pools at the end of the experiment. Working across three stream systems and with an impressive level of replication, the researchers observed a strong pattern of elevated mating and reproductive success for whichever male type was rare.
Although this is an important study, it is not without limitations. One potential issue stems from the fact that, in guppies, fertilization is internal, and females can store sperm for weeks or months. When Hughes et al. collected females from their experimental pools and allowed the fish to give birth in the lab, they found strong evidence for a rare-male effect among the fathers of the first round of offspring. But when the females were obliged to use stored sperm for a second brood, the rare-male effect among the fathers of those offspring was not statistically significant. The authors argue that, in nature, female guppies mate frequently and rarely rely on stored sperm, so that all natural broods are essentially equivalent to the first broods in their experiment. However, the data reviewed by Hughes and colleagues in support of this claim are not extensive, and more work on this point would be helpful.
There was also a technical limitation in the genotyping technique used by the authors: relying on variable genomic regions known as microsatellites, they could confidently assign paternity to only a minority of individual offspring. Although there is no reason to expect this to create any bias in the data, it might be worthwhile revisiting the samples as more powerful methods for assigning paternity become available.
Hughes and colleagues' evidence for the rare-male effect in nature raises intriguing questions. The most obvious is, why do female guppies prefer males with uncommon colour patterns? Here we have more hypotheses than data sets. One theoretical analysis suggests that greater survival of rare male types, which has been found in guppies2, might contribute to the evolution of such a preference, even if it is costly9. Interestingly, the same analysis points out that the negative feedback inherent in sexual selection for rarity (such selection causes rare types to become common) can ultimately prevent preferences for rare males from becoming ubiquitous. It remains to be determined whether preference for rarity varies among guppy females in experimental populations such as those used in this study. Hughes et al. point out that the rare-male effect might also emerge if females avoid mating with males that share the colour patterns of their previous mates, to increase the genetic diversity of their offspring. Alternatively, preferences for rarity could have evolved because they lead to lower rates of inbreeding if populations are small and intermittently isolated. It has even been suggested10 that mating preferences for rare types provide no benefit for females and may be a manifestation of a preference for novelty that has evolved in other contexts.
The clever manipulations of natural populations used by Hughes et al. may, as the authors suggest, be a promising avenue for exploring the maintenance of variation by frequency-dependent selection in other systems. It might well be the case that, when put to the test, preferences for rarity might themselves not prove to be so rare.
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McKinnon, J., Servedio, M. Novelty makes the heart grow fonder. Nature 503, 44–45 (2013). https://doi.org/10.1038/nature12701