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...
Assessment strategies are an important component in game theoretical models of contests. Strategies can be either based on one’s own abilities (self assessment) or on the relative abilities of two opponents (mutual assessment). Using statistical methodology that allows discrimination between assessment types, we examined contests in the jumping spider Phiddipus clarus. In this species, aggressive interactions can be divided into ‘pre-contact’ and ‘contact’ phases. Pre-contact phases consist of bouts of visual and vibratory signaling. Contact phases follow where males physically contact each other (leg fencing). Both weight and vibratory signaling differences predicted winners with heavier and more actively signaling males winning more contests. Vibratory behaviour predicted pre-contact phase duration, with higher signaling rates and larger differences between contestants leading to longer pre-contact interaction times. Contact phase duration was predicted most strongly by the weight of losing males relative to that of winning males, suggesting that P. clarus males use self-assessment in determining contest duration. While a self-assessment strategy was supported, our data suggest a secondary role for mutual assessment (“partial mutual assessment”). After initial contest bouts, male competitors changed their behaviour. Pre-contact and contact phase durations were reduced while vibratory signaling behaviour in winners was unchanged. In addition, only vibratory signaling differences predicted winners in subsequent bouts suggesting a role of experience in determining contest outcomes. We suggest that the rules and assessment strategies males use can change depending on experience and that assessment strategies are likely a continuum between self- and mutual assessment.
One of the key challenges of both ecology and evolutionary biology is to understand the mechanisms that maintain diversity. Negative frequency-dependent selection is a powerful mechanism for maintaining variation in the population as well as species diversity in the community. There are a number of studies showing that this type of selection, where individuals of a rare type (i.e. a rare morph or a rare species) experience higher survival than those of more common type(s). However, it is still not clear how frequency-dependent selection operates. Search image formation has been invoked as a possible, proximate explanation. Although the conceptual link between search image and frequency-dependent predation is often assumed in ecological and evolutionary studies, a review of the literature reveals a paucity of evidence demonstrating the occurrence of both in a natural predator-prey system. Advances in the field of psychology strongly support the existence of search image, yet these findings are not fully recognized in the realm of ecology and evolutionary biology, in part, we feel because of confusion and inconsistencies in terminology. Here we try to simplify the language, clarify the advances in the study of frequency-dependent predation and search image, and suggest avenues for future research. We feel that the investigations of both proximate (perceptual mechanisms) and ultimate (pattern of predation) processes are necessary to fully understand the importance of individual behavioural processes for mediating evolutionary and ecological diversity.
Sexually antagonistic genetic variation can pose limits to the independent evolution and adaptation of the sexes. The extent of sexually antagonistic variation is reflected in the intersex genetic correlation for fitness (r w FM ). Previous estimates of this correlation have been mostly limited to populations in environments to which they are already well adapted, making it difficult to gauge the importance of sexually antagonistic genetic variance during the early stages of adaptation, such as that occurring following abrupt environmental change or upon the colonization of new habitat. Here we assayed male and female lifetime fitness in a population of Drosophila serrata in four novel laboratory environments. We found that r w FM varied significantly across environments, with point estimates ranging from positive to negative values of considerable magnitude. We also found that the variability among estimates was because, at least in part, of significant differences among environments in the genetic variances of both male and female fitness, with no evidence of any significant changes in the intersex covariance itself, although standard errors of these estimates were large. Our results illustrate the unpredictable nature of r w FM in novel environments and suggest that, although sexually antagonistic genetic variance can be pronounced in some novel environments, it may have little effect in constraining the early stages of adaptation in others.
Sexual dimorphism in coloration is a taxonomically widespread phenomenon often attributed to sexual selection on visual signals. However, the ambush bug Phymata americana exhibits sexual dimorphism in coloration that has no apparent signalling function. Here we provide evidence that colour pattern in this species influences male mating success indirectly through its effect on thermoregulation. We demonstrate, using experimental manipulation, that individuals with dark colour pattern achieve higher thoracic temperatures under illumination. We also show that dark colour pattern predicted mate-searching success but only under thermally challenging conditions (i.e. cool ambient temperature). As far as we are aware, this is the first study to provide evidence that sexual dimorphism can be accounted for by sexual selection on thermoregulatory performance.
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