Revealing the trade-off between resistance and maintenance under sexual conflict

New research pub­lished in Evol­u­tion Let­ters demon­strates that in fruit flies, female res­ist­ance to sexu­al con­flict is depend­ent on food avail­ab­il­ity. Lead author of the study, Dr Wayne Rostant, tells us more.

In spe­cies which repro­duce sexu­ally, i.e. either with sep­ar­ate sexes (or sex func­tions in the case of herm­aph­rod­ites) it is com­mon to find that life-his­tor­ies and strategies that would optim­ise female evol­u­tion­ary suc­cess are quite dif­fer­ent to those which optim­ise male evol­u­tion­ary suc­cess. The traits upon which these optim­al strategies are based are very often shared by males and females, how­ever, set­ting up a ten­sion between the sexes. This res­ults in what is known as sexu­al con­flict, defined broadly as sexu­ally ant­ag­on­ist­ic selec­tion on shared traits. One com­mon example of this is the con­flict seen in many spe­cies over mat­ing rate, where the optim­al rate for males far exceeds that for females. In oth­er words, males can max­im­ise their life­time repro­duct­ive out­put by mat­ing often where­as females max­im­ise their out­put by mat­ing one or a few times. Sexu­al con­flict is revealed in the evol­u­tion­ary to and fro of adapt­ive response and counter response described as an evol­u­tion­ary ‘arms race’ between the sexes. An adapt­ive response to selec­tion which favours males but harms females could res­ult in the evol­u­tion of coun­terad­apt­a­tions in females to min­im­ize the poten­tially costly side effects.

How­ever, this evol­u­tion­ary ‘arms race’ doesn’t hap­pen with­in a vacu­um. Eco­lo­gic­al con­text is import­ant. Organ­isms need to sur­vive to repro­duce and, giv­en the neces­sary ener­get­ic trade-offs inher­ent in life-his­tory the­ory, we should recog­nize and emphas­ize the influ­ence of resource levels and con­di­tion depend­ence (i.e. how sens­it­ive traits are to resource levels) when we exam­ine sexu­al con­flict.  This is of fun­da­ment­al import­ance because resource levels may sig­ni­fic­antly influ­ence and even reverse the out­comes of sexu­al con­flict. How­ever, to date, we lack empir­ic­al tests of this key idea.

This motiv­ated our research on the effects of diet on the evol­u­tion­ary out­comes of elev­ated court­ship and mat­ing with­in the fruit fly Dro­so­phila melano­gaster. The observed costs of mat­ing in female fruit flies is a rel­at­ively well-known example of sexu­al con­flict. Past work by Dr Stu­art Wigby and Pro­fess­or Tracey Chap­man (Oxford Uni­ver­sity) had shown that an evol­u­tion­ary his­tory of elev­ated sexu­al con­flict can lead to the evol­u­tion of res­ist­ance to costs of mat­ing in females. In this scen­ario, females exposed over time to elev­ated court­ship and mat­ing fre­quen­cies evolve the abil­ity to ameli­or­ate these effects such that they can express high­er sur­viv­al when con­tinu­ally exposed to males. In a replay of that exper­i­ment we set up vari­ous fruit fly pop­u­la­tions in which we manip­u­lated the adult sex ratio to either be male-biased, equal-sex ratio or female-biased. These treat­ments are prox­ies for high-con­flict, medi­um-con­flict and low con­flict respect­ively, as they res­ult in females exper­i­en­cing cor­res­pond­ingly high, medi­um and low rates of court­ship and mat­ing. The key elab­or­a­tion this time around involved a sim­ul­tan­eous manip­u­la­tion of adult resource levels where half of the pop­u­la­tions were giv­en a high yeast diet and the oth­er half a low yeast diet. We then allowed these pop­u­la­tions to evolve under these manip­u­la­tions for sev­er­al gen­er­a­tions before con­duct­ing life-his­tory tests at dif­fer­ent time-points.

Obser­va­tion of in-situ (that is, in the pop­u­la­tion cages) beha­viour showed no effect of the resource levels on the amount of atten­tion received by females, thus allow­ing us to test, in well-adap­ted pop­u­la­tions exper­i­en­cing ostens­ibly sim­il­ar selec­tion pres­sures, the hypo­thes­is that resource levels con­strain female responses to elev­ated sexu­al con­flict. High-con­flict females from rich-resource regimes, uncon­strained by trade-offs with somat­ic main­ten­ance, were expec­ted to have the capa­city to express res­ist­ance responses. In con­trast, under poor resource regimes, such females are expec­ted to evolve res­ist­ance to sexu­al con­flict only by trad­ing it off against somat­ic main­ten­ance i.e. the busi­ness of simply sur­viv­ing. Hence, our first pre­dic­tion was that elev­ated sexu­al con­flict would restrict the evol­u­tion of male harm res­ist­ance to resource-rich regimes, because only in these would females have the capa­city to respond to selec­tion by invest­ing in somat­ic main­ten­ance and res­ist­ance. The gen­er­al lack of male sur­viv­al responses to sexu­al con­flict observed in the pre­vi­ous Wigby and Chap­man study and the find­ing that life his­tory traits in males can show lim­ited responses to prox­im­ate diets gen­er­ated a second pre­dic­tion: that the out­comes would be sex specific.

We tested these pre­dic­tions with stand­ard­ized assays on flies des­cen­ded from these exper­i­ment­al evol­u­tion pop­u­la­tions. We determ­ined lifespan, age­ing, and fit­ness for both sexes of each regime under “no con­flict” (once mated individuals—to reveal invest­ment in baseline somat­ic main­ten­ance) and “con­flict” (con­tinu­ally mated individuals—to indic­ate invest­ment in res­ist­ance) con­di­tions. Con­sist­ent with the Wigby and Chap­man study, in resource-rich regimes the high-con­flict females evolved res­ist­ance to con­tinu­al expos­ure to males, being longer-lived than low-con­flict females when tested in the “con­flict” assay.  Under the “no-con­flict” con­di­tions there was no dif­fer­ence in baseline sur­viv­al, con­sist­ent with the idea that responses evolving under nutri­tion­al abund­ance exper­i­enced no trade-offs with res­ist­ance. This con­tras­ted with the res­ults from the poor resource regimes, where the abil­ity of high-con­flict females to evolve res­ist­ance to males was severely com­prom­ised and they also showed lower baseline sur­viv­al than low-con­flict females. This sug­ges­ted high con­flict females traded off somat­ic main­ten­ance against any lim­ited res­ist­ance they had evolved in response to sexu­al con­flict. As pre­dicted, we also found males gen­er­ally unre­spons­ive to the sex-ratio and resource treatments.

Over­all, these find­ings provide exper­i­ment­al sup­port for the hypo­thes­is that evol­u­tion­ary responses to sexu­al con­flict are crit­ic­ally depend­ent upon resource levels. Spe­cific­ally, we have shown that resource avail­ab­il­ity can con­strain the expres­sion of responses to elev­ated sexu­al con­flict and in doing so reveal under­ly­ing trade-offs. The work high­lights the key, gen­er­al role of resources such as food in determ­in­ing the expres­sion of responses to selection.

Dr Wayne Rostant is an evol­u­tion­ary bio­lo­gist at the Uni­ver­sity of East Anglia. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Let­ters.