Genetic basis of female sexual preference in a stalk-eyed fly

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There is considerable interest amongst the general public and scientists in understanding how exaggerated male sexual ornaments have evolved through female mate preferences. Much recent interest in sexual selection has been directed toward understanding the causes of variation in male ornaments, both genetic and environmental, and the signalling value of these traits. In contrast, there has been a neglect of in depth studies of variation in female sexual preferences. This in part reflects the difficulty of accurately quantifying preferences - which requires repeated measures of female responses to a variety of male stimuli, which are often difficult to study under laboratory conditions. It also reflects a general under appreciation of the variability and complexity of female preference behaviour. We have already developed an excellent system for quantifying variation in female mate preference in the African stalk-eyed fly Diasemopsis meigenii. In this species, females actively reject unwanted male mating attempts. This has allowed us to develop protocols to accurately measure individual female mate preferences. We have previously demonstrated that the strength of preference varies positively with phenotypic variation in female eyespan and female fecundity. A key question to address is the genetic underpinnings of variation in female mate preferences. Without genetic variation female preference cannot evolve. We will carry out the first QTL (quantitative trait locus) study of the genetics of preference. This will uncover the number of separable genetic factors underlying variation in preference. It may be that there are one or two genetic factors with major effects or alternatively a more even distribution of effect sizes of genes across the genome. It will also reveal the linkage pattern of preference genes and whether there is a bias towards the X-chromosome, as some theory predicts. Another critical issue that we will investigate is the evidence that preferences are condition-dependent. Several recent studies have shown that females reared under good conditions in which high quality resources are freely available have different preferences than females reared on poor quality resources. For example, in our previous work, we have shown that female stalk-eyed flies with access to better larval or adult resources have stronger directional preferences for males with larger sexual ornaments. This has wide ranging implications for the strength of sexual selection, if the females with the highest condition not only show the greatest discrimination of who they mate with but are also the most fecund. We will investigate the genetics of condition-dependent preferences using a quantitative genetic study. Genetically related families will be raised in three environments which vary in food quality. It is possible that the environmental variation will overwhelm the genetic signal. But from our previous studies measuring the responses of male traits to environmental stress, we do not expect this. Rather we believe that the harsh environment will amplify genetic differences between females, bringing out genetic variation in preference. So some female genotypes will consistently produce strong preference in all environments, whereas others genotypes will show declining preference as environmental conditions deteriorate. We will further probe this prediction in our QTL study. We have already shown that the strength of female preference in stalk-eyed flies covaries with female eyespan and female fertility, two traits that strongly reflect resources available during larval and adult development respectively. We will test whether QTL for female preference are located in the same genomic regions as QTL for female eyespan and QTL for female fecundity. This pattern could indicate that the same genes for condition underlie several traits such as preference, eyespan and fecundity.