Frequency-dependent survival in natural guppy populations

Abstract

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology [1][2][3] . Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory 1 ; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata) 4,5 . Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans 6,7 and other species 8,9 implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival-an evolutionary process capable of maintaining extreme polymorphism.Colour-pattern polymorphism in guppies is limited to males and consists of irregular spots of several different structural (blue, green and purple) and pigment-based (yellow, orange, red and black) colours that occur on the body, caudal fin and dorsal fin (Fig. 1). The position, number, size and hue of the spots are highly heritable 5,10 , although the colour saturation (chroma) of orange spots can be influenced by diet 11,12 . Male colouration is highly polymorphic despite being subject to sexual and ecological selection. Female mating preferences usually favour males with the greatest area of orange, although the strength of that preference varies among populations 10,12,13 . Predators also exert selection on colour patterns; they preferentially prey upon males with brighter or more conspicuous colours 14,15 . Despite the apparently strong and directional selection within populations, colour patterns are so variable that any two males are easily distinguishable based on colour pattern alone, unless they are closely related 10 .Several mechanisms have been proposed to explain the maintenance of this extreme polymorphism 10,14 . Mate-choice experiments indicate that females preferentially mate with males bearing rare or novel colour patterns 16,17 . A trade-off (antagonistic pleiotropy) between male sexual attractiveness and offspring viability has also been reported 18 . Both processes could contribute to the maintenance of genetic variation in nature. However, experiments demonstrating these processes were conducted in laboratory environments, and it is not clear whether either process occurs in nature. Another process capable of maintaining polymorphism is a rare-morph survival advantage. This process has been implicated in the maintenance of colour polymorphism in some invertebrates 19,20 and vertebrates 21 , but it has not been tested in the highly polymorphic guppy system. We tested the hypothesis that ma...

Size-dependent colouration in larvae of Orgyia antiqua (Lepidoptera: Lymantriidae): A trade-off between warning effect and detectability?

“…It is notable, however, that unlike the later switch from bright to dull, there is a wide range of body weights at which both pied and bright morphs occur at an approximately equal frequency. Such a pattern of seemingly random, stabile coexistence may be consistent with the scenario of frequency dependent selection maintaining stabile polyphenism, either on a genetic basis (Olendorf et al, 2006), or as a result of a coin-flipping plasticity (Cooper & Kaplan, 1982;Meyers & Bull, 2002). An advantage of being different from the majority, indeed, is expected in this system, as larval densities are often high in O. antiqua (e.g.…”

Male harassment drives females to alter habitat use and leads to segregation of the sexes

“…Levels of male harassment are high in this species (Magurran & Seghers 1994) and previous work has shown that in wild guppy populations inhabiting rivers with a high risk of predation by piscivorous fishes, the sexes segregate in the habitat such that areas of the river with the highest predation risk (deep water) have female-biased sex ratios and areas with the lowest predation risk (shallow water) are male biased (Croft et al 2006). Guppies are highly sexually dimorphic with males being small and brightly coloured and females being large and cryptically coloured, making males more conspicuous to aquatic predators (Olendorf et al 2006). Deep water in rivers with large piscivorous fishes is thus less optimal habitat for male than for female guppies due to this sexual dimorphism; however, females would still be at lower risk from aquatic predators in shallower water.…”

Heterospecific aggression bias towards a rarer colour morph

“…Even in the absence of any performance advantages, one might expect the type of variation represented by discrete morphs to simply erode from the population through genetic drift and other random events [7,8]. However, morph coexistence can be favoured if a rarer morph has an advantage that is tempered at higher frequencies [9][10][11][12][13].…”