Determining the genetic basis of sexual conflict in Drosophila melanogaster: the role of the sex peptide.

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

Sexual conflict is a revolutionary way of viewing what happens between males and females over reproductive decisions. Rather than co-operating over who to mate with, how often to mate, how many offspring to produce and how much parental care to give, the sexes instead often disagree, and try to exploit one another for their own ends. Examples of this 'sexual conflict' have been described in many different organisms, but have been most intensively studied in the insects. In the fruitfly Drosophila melanogaster, there is strong conflict between the sexes over how often to mate. A high frequency of mating best suits males, as they provide no parental care and thus each extra mating results in them fathering more offspring. The interests of females are best served by a lower frequency of mating - they have a limited number of eggs to lay and beyond a certain level of remating, they gain no further increases in offspring numbers, Furthermore, high frequencies of mating are costly to females, shortening their lifespans and lowering their overall lifetime reproduction. Our previous work has revealed that these 'mating costs' in females are caused by the actions of molecules in the male semen, which are transferred to females during mating. We have recently identified a substance known as the 'sex peptide' which is responsible for the female mating costs, and matings with males that lack this peptide are 'cost-free' for females. Males benefit from the transfer of the sex peptide because one of its functions is to render females temporarily unwilling to mate again, hence males who transfer it father more offspring. The sex peptide therefore simultaneously harms females and benefits males and is the first gene product shown to underlie sexual conflict in any species. Our discovery prompts many questions: e.g. how does the SP harm females?, are females equally sensitive to it throughout their lives? and is the damage caused by the sex peptide permanent? We address these questions in the work proposed here. We have three broad aims and these are (1) to quantify the extent to which the sex peptide underlies sexual conflict, (2) to reveal how sex peptide exerts harm on females and (3) to measure how the costs and benefits of receiving the sex peptide are affected by mating rate and by variations in food supply. We will do large-scale experiments in the laboratory, using healthy flies. This will allow us to detect subtle differences and to estimate accurately 'fitness' (a combination of survival and reproductive output). To manipulate the level of sex peptide that females receive we will mate them to normal males or those which lack the sex peptide. The results will provide an in depth analysis, for the first time, of the basis of sexual conflict at the genetic level. The general benefits of the research will be to deepen our understanding of the evolution of sexual conflict, by understanding the nature and dynamics of the conflicts between males and females. This will allow us to better understand how reproductive strategies evolve in males and females. There are also wider potential applications in insect pest control. For example, in many parts of the world the true' fruit flies are pests. The females lay their eggs in ripe fruit, which is spoiled as the larvae develop. These pests are often controlled using the 'sterile insect technique' (SIT). In this, males are reared on a large scale in factories, sterilised and then released into the environment to mate with the wild females. Such matings are sterile and the pest population size is thus reduced. SIT works best if females do not mate again, and sex-peptide-like factors appear to play a crucial role in this. Hence manipulating the level of sex peptide-like factors could provide improvements in pest suppression in insects subjected to SIT.

Publications

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Chapman T (2008) Evolutionary biology: sterile saviours. in Current biology : CB

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Edward DA (2010) Adaptations to sexual selection and sexual conflict: insights from experimental evolution and artificial selection. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Edward DA (2011) Quantifying the life-history response to increased male exposure in female Drosophila melanogaster. in Evolution; international journal of organic evolution

 
Description Sexual conflict is seen when the interests of males and females over reproductive decisions diverge. Rather than co-operating over who to mate with, how often to mate, how many offspring to produce and how much parental care to give, the sexes instead often disagree, and try to exploit one another for their own ends.



In the fruitfly there is strong conflict between the sexes over how often to mate. A high frequency of mating suits males, as they provide no parental care and therefore each extra mating results in more paternity. The interests of females are best served by a lower frequency of mating - they have a limited number of eggs to lay and beyond a certain level of remating, they gain no further increases in offspring numbers. Furthermore, high frequencies of mating are costly to females, shortening their lifespans and lowering their overall lifetime reproduction. Our previous work revealed that these 'mating costs' in females are caused by the actions of molecules in the male semen, particularly a substance known as the 'sex peptide' (SP). Based upon these initial data, we launched here a study that had 3 broad aims, and these - together with the main findings - are outlined below.



(1) To quantify the extent to which SP underlies sexual conflict.

SP is important in mediating sexual conflict because receipt of this molecule by females decreases their lifespan and success in reproduction. In the present project we showed that SP acts to increase male reproductive success by significantly increasing the relative and absolute number of progeny that males father before their mates pair off with other males. This is because SP delays remating and boosts the number of offspring produced in the period between matings. We also conducted a transgenerational study, to show the effects in males and females, of the expression of high and low mating costs in female parents, grand and great grant parents.



(2) To reveal how SP exerts harm on females.

We identified, using a combination of theory and experimental data, the stage in the life of a female the effects of SP are most apparent. We showed that the impacts of mating are felt most keenly in young females under conditions when populations are expanding. We also investigated whether the effects of mating on female lifespan and reproductive success were reversible or whether they exposed females to more risk: the answer appears to be both.



(3) To measure how the costs and benefits of receiving the sex peptide are affected by mating rate and by variations in food supply.

A major finding was that the amount of food available to either males or females affected their ability to cause SP responses or to respond to them. This is important as it shows how resource levels can alter how often interactions between males and females are mutually beneficial and how often they are typified instead by sexual conflict. The work also highlights how there is a continuum between these two outcomes and how the exact outcome is determined by the balance between the costs and benefits of male mating adaptations that have potentially costly effects.



Overall we gained a significantly better understanding of how reproductive strategies evolve. Our work also feeds into insect pest control. For example, in many parts of the world the true fruit flies are pests. The females lay their eggs in ripe fruit, which is spoiled as the larvae develop. These pests are often controlled using the 'sterile insect technique' (SIT). In this, males are reared on a large scale in factories, sterilised and then released into the environment to mate with the wild females. Such matings are sterile and the pest population size is thus reduced. SIT works best if females do not mate again, and SP-like factors appear to play a crucial role in this. Hence manipulating the level of sex peptide-like factors could potentially provide improvements in pest suppression in insects subjected to SIT.
Sectors Environment