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

Lead Research Organisation: University College London
Department Name: Genetics Evolution and Environment

Abstract

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.

Publications

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Chapman NC (2017) The complexity of mating decisions in stalk-eyed flies. in Ecology and evolution

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Cotton S (2009) Eyespan reflects reproductive quality in wild stalk-eyed flies in Evolutionary Ecology

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Finnegan S (2019) Does meiotic drive alter male mate preference? in Behavioral Ecology

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Hadjivasiliou Z (2012) Selection for mitonuclear co-adaptation could favour the evolution of two sexes. in Proceedings. Biological sciences

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Hadjivasiliou Z (2016) The evolution of mating type switching. in Evolution; international journal of organic evolution

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Hadjivasiliou Z (2016) Gamete signalling underlies the evolution of mating types and their number. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

 
Description This project focused on aspects of female mate preference and the male ornamental trait (eyespan) in an African stalk-eyed fly. This is a model species for the study of sexual selection because females are known to prefer to mate with males of large eyespan and are able to actively reject unwanted suitors. The project combined phenotypic manipulation and genomic techniques.

A main outcome was that we identified and mapped quantitative trait loci (QTL) for mate preference in the stalk-eyed fly. We generated a suite of highly inbred lines that differed in female preference and other key traits. These lines were exploited to enable the identification, sequencing and evaluation of a suite of single nucleotide polymorphisms (SNPs) to create a genomic map. Subsequently we made a linkage map and conducted a mapping experiment to search for QTL underpinning the expression of a suite of traits, using an F2 cross between high- and low-preference inbred lines. We found QTL for morphological traits (including male and female eyespan), female fecundity, and female rate of rejection of unwanted males.

A further discovery was that the sexually selected exaggerated male trait (eyespan) of the study species was especially sensitive to genetic stress and that variation in the eyespan phenotype was a reliable predictor of extinction risk in small populations. These findings were based on a long-term study of the effects of 11 generations of full-sib mating on sexual and non-sexual traits.

An in-depth analysis of the complexity of mating decisions in the study species revealed the importance of evaluating multiple traits in males and females, not just the most obvious exaggerated and sexually dimorphic traits. This was based on measuring how female acceptance or rejection of prospective mates was affected by variation in attributes such as female eyespan, male reproductive traits and male behaviour directed towards females.
Exploitation Route The findings will be of direct interest to researchers in evolutionary biology, plant and animal breeders and environmental science. Future research ought to focus on further dissection of the interplay between males and females over mating decisions and outcomes, and consideration of genetic differences between stalk-eyed fly species.
Sectors Education

 
Description Mapping sexual traits in a stalk-eyed fly 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Postgraduate students
Results and Impact After the research seminar, question and answer session with audience about the experimental designs.

Greater awareness of research in sexual selection.
Year(s) Of Engagement Activity 2012