The ecology of sexual conflict: Temperature variation in the social environment can drastically modulate male harm to females

Abstract

Sexual conflict is a fundamental driver of male/female adaptations, an engine of biodiversity and a crucial determinant of population viability. Sexual conflict frequently leads to behavioural adaptations that allow males to displace their rivals, but in doing so harm those same females they are competing to access, which can decrease population viability and facilitate extinction. We are far from understanding what factors modulate the intensity of sexual conflict and particularly the role of ecology in mediating underlying behavioural adaptations. In this study, we show that, in Drosophila melanogaster, variations in environmental temperature of ±4°C decrease male harm impact on female fitness by between 45% and 73%. Rate‐sensitive fitness estimates indicate that such modulation results in an average rescue of population productivity of 7% at colder temperatures and 23% at hotter temperatures. Our results: (a) show that the thermal ecology of social interactions can drastically modulate male harm via behavioural plasticity, (b) identify a potentially crucial ecological factor to understand how sexual conflict operates in nature and (c), along with recent studies, suggest that behaviourally plastic responses can lessen the negative effect of sexual conflict on population viability in the face of rapid environmental temperature changes. A plain language summary is available for this article.

Plasticity in male mating behavior modulates female life history in fruit flies

“…; García‐Roa et al. ). We add to these findings by documenting that the perception of sperm competition risk in a male's social environment can elicit phenotypic changes in his mating behavior that have significant consequences for their mates’ life histories.…”

“…These studies suggest that environmental factors such as space availability and complexity, predation risk, and population density can modulate the expression and/or evolution of sexually antagonistic traits and thus the magnitude of male-induced harm (Yun et al 2017;Gomez-Llano et al 2018;García-Roa et al 2019). For example, García-Roa et al 2019) demonstrated that plasticity in male-induced harm can be modulated by temperature, whereby females exposed to males at 29°C had shorter lifespans and fewer lifetime offspring compared to females that mated with males at 25°C or 21°C. Although these studies highlight the importance of considering a broad range of socioecological factors when measuring the intensity of sexual conflict, to the best of our knowledge, no experimental studies have tested how the modulation by social experience of male reproductive traits influences the magnitude of male-induced harmful effects on females.…”

“…For example, García‐Roa et al. ) demonstrated that plasticity in male‐induced harm can be modulated by temperature, whereby females exposed to males at 29°C had shorter lifespans and fewer lifetime offspring compared to females that mated with males at 25°C or 21°C. Although these studies highlight the importance of considering a broad range of socioecological factors when measuring the intensity of sexual conflict, to the best of our knowledge, no experimental studies have tested how the modulation by social experience of male reproductive traits influences the magnitude of male‐induced harmful effects on females.…”

“…In the past few years, several studies have highlighted the importance of considering these socioecological effects when quantifying the intensity of sexual conflict (Perry and Rowe 2018). These studies suggest that environmental factors such as space availability and complexity, predation risk, and population density can modulate the expression and/or evolution of sexually antagonistic traits and thus the magnitude of male-induced harm (Yun et al 2017;Gomez-Llano et al 2018;García-Roa et al 2019). For example, García-Roa et al 2019) demonstrated that plasticity in male-induced harm can be modulated by temperature, whereby females exposed to males at 29°C had shorter lifespans and fewer lifetime offspring compared to females that mated with males at 25°C or 21°C.…”

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

“…These results suggest that abiotic factors experienced during development might influence the dynamics of sexual conflict among adults and illustrates that adopting a biogeographic perspective can be fruitful to understand such evolutionary dynamics. The study of sexual conflict has been heavily dominated by laboratory studies of model organisms in controlled and stable laboratory environments (Rice ; Arnqvist & Rowe ) but recently the role of temperature, climate and other ecological factors in modulating various forms of sexual conflict has gained increased attention (Berger et al ; Perry et al ; De Lisle et al ; García‐Roa et al ). The novel results in this study suggest that temperature can also influence the morph frequency composition among adults through frequency‐independent pre‐reproductive selection operating earlier in ontogeny.…”