Symposium: “Sexual conflict: Mechanisms and emerging themes in resistance biology”

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Tracey Chapman (Aug 2018)

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Females may have to receive many different types of signals and messages from males during mating (represented by the different sizes, shapes and shades of arrows). Males may use highly complex sets of signals as part of a strategy to make it difficult for females to evolve resistance against those signals.
(Credit: Tracey Chapman)

Battles between the interests of males and females over reproductive decisions, such as how often to mate and how much to invest now versus later, are widespread. Much progress has been made over the past few decades in understanding why and how these battles occur. Broadly speaking, in situations where reproducing partners have little shared interest in each other’s reproductive futures, they can sometimes benefit by exploiting, rather than fully cooperating with, their mates. Much work into the details of how these sexual conflicts are manifested has been done in insects, due to their ease of study and manipulation. In particular, studies on Drosophila fruitflies has revealed a fascinating covert battleground between males and females mediated by the actions of seminal fluid proteins passed from males to females during mating along with sperm. These proteins affect the behavior and physiology of the female in dramatic ways by altering her egg laying, sexual receptivity, feeding, and immune genes. Males can sometimes gain by using these proteins to make females invest more in current versus future reproductive episodes, even though this can be harmful to females in the longer term, e.g. by shortening their lifespan. In this situation, females should evolve resistance to these proteins to avoid this harm. A stand-out feature of seminal fluid proteins involved in mediating sexual conflict is their complexity. In this article, the idea is explored that this complexity arises in part as a strategy to allow males to effectively manipulate the reproductive system of females in a way that makes it hard for females to resist. This idea comes from examining parallels with the strategies employed by humans to slow the evolution of resistance to pesticides and antimicrobial drugs. Strategies in which males employ multiple manipulative pathways across time and space are predicted to be the most effective at slowing female counter responses. Thinking about the problem in this way may provide a new way in which to study the manipulative strategies of males towards females and specifically to explain why some male strategies are ‘resistance proof’ and hence persist, while others aren’t and don’t.


Abstract

Sexual conflict is acknowledged as pervasive, with the potential to generate and maintain genetic variation. Mechanistic studies of conflict have been important in providing direct evidence for the existence of sexual conflict. They have also led to the growing realization that there is a striking phenotypic diversity of adaptations whose evolution can be shaped by sexually antagonistic selection. The mechanisms involved range from the use of genital spines, claspers, songs, smells to ejaculate molecules. In one well-studied example, sexual conflict can occur over the sexually antagonistic effects of seminal fluid proteins in Drosophila melanogaster. However, an important puzzle remains, namely why seminal fluid proteins are so numerous and complex, hence whether all or some are involved in mediating sexual conflict. I hypothesize that this rich diversity, and the complexity of traits subject to sexually antagonistic selection in general, may arise, at least in part, due to the deployment of sexually antagonistic adaptations in males in a way that lessens the probability of broad scale, strong resistance evolution in females. In elaborating this hypothesis I explore how research into the evolution of resistance to insecticides, antimicrobials and vaccines might be used to provide insights into the evolution of female resistance to the effects of sexually antagonistic manipulative traits of males. In this manner, the manipulative traits of males can be resistance-proofed.