The battle between the sexes

A new study pub­lished in Evol­u­tion Let­ters has shown that female fruits flies can alter their repro­duct­ive beha­viour to exert con­trol over patern­ity suc­cess of dif­fer­ent males. Lead author Dr Meghan Laturney tells us more.

Sexu­al rela­tion­ships can be very com­plic­ated. Part of this com­plex­ity is born out of the fact that sexu­al repro­duc­tion, like any social beha­viour, is a com­bin­a­tion of both cooper­a­tion and con­flict. From an evol­u­tion­ary per­spect­ive, sex is fun­da­ment­ally a cooper­at­ive beha­viour. The only way for a sexu­ally repro­du­cing indi­vidu­al to have any repro­duct­ive suc­cess is to make off­spring; and in most cases this requires cop­u­la­tion with the appro­pri­ate social part­ner. When males and females cop­u­late, both the indi­vidu­al and their part­ner are work­ing towards a col­lect­ive goal: to pro­duce off­spring togeth­er to res­ult in increased per­son­al repro­duct­ive suc­cess. Cop­u­la­tion is cooper­a­tion since it res­ults in mutu­al gain.

How­ever, it’s not just about get­ting some repro­duct­ive suc­cess – it’s about max­im­iz­ing your repro­duct­ive suc­cess. One com­mon way to increase either the quant­ity or qual­ity of off­spring pro­duced is to mate more often with dif­fer­ent part­ners. In gen­er­al, this is true for both males and females and applies to vari­ous spe­cies across the anim­al king­dom. Even in groups that are socially mono­gam­ous (males and females pair bond and raise young togeth­er), many off­spring are pro­duced from non-pair bon­ded par­ents, sug­gest­ing that sexu­al promis­cu­ity is the rule rather than the excep­tion. Females, how­ever, are lim­ited in the num­ber of off­spring they can pro­duce by the num­ber of eggs they devel­op – a restrain­ing factor not shared with males. This makes it much more likely that female remat­ing (poly­andry) is advant­age­ous because it increases the genet­ic diversity of the brood (group of off­spring) rather than a bump in brood number.

But how does this increased sexu­al beha­viour impact the off­spring pro­duc­tion of pre­vi­ous mates? Well, it depends heav­ily on the spe­cies’ mat­ing sys­tem; how­ever, gen­er­al­iz­a­tions can be made. It’s often the case that although male remat­ing (poly­gyny) has little impact on the suc­cess of females, poly­andry on the oth­er hand sig­ni­fic­antly lowers the sir­ing cap­ab­il­ity of her pre­vi­ous male mates. This makes sense when we are reminded that when females remate in quick suc­ces­sion, the sperm of her mates will coex­ist with­in the same repro­duct­ive tract com­pet­ing for fer­til­iz­a­tion of a lim­ited num­ber of eggs. Put­ting it togeth­er, poly­andry presents a con­flict between the sexes as it is bene­fi­cial for females but costly for males.

In the face of sexu­al con­flict, males are pre­dicted to devel­op ways to increase their off­spring pro­duc­tion. That means if females are going to remate, then males should be pre­pared to com­pete for fer­til­iz­a­tion suc­cess with­in female repro­duct­ive tract. Indeed, many research­ers have repor­ted instances of tac­tics of sperm com­pet­i­tion: char­ac­ter­ist­ics expressed by the male or the sperm that increase the chances of his sperm fer­til­iz­ing the egg. As a res­ult of sperm com­pet­i­tion, brood patern­ity of a mul­tiply-mated female is not equal across mates. In fact, a likely out­come for many ver­teb­rate and inver­teb­rate spe­cies alike is a bias in brood patern­ity in favour of the last male, a phe­nomen­on known as last male sperm pre­ced­ence. In oth­er words: one male wins or at least wins major­ity. Although this out­come is rather ideal for the last male, it also res­ults in an over­all reduc­tion in the brood genet­ic diversity, which is hypo­thes­ised to be a bene­fit to the female and a driv­ing factor for the pre­val­ence of polyandry.

Fol­low­ing the logic that sug­ges­ted the devel­op­ment of male tac­tics of sperm com­pet­i­tion, sexu­al con­flict the­ory would also sug­gest that females devel­op counter-adapt­a­tions to reduce last male sperm pre­ced­ence and restore max­im­um diversity. How­ever, there has been very little atten­tion on female con­trol of repro­duc­tion. Unlike oth­er sys­tems that show sim­il­ar co-evol­u­tion such as para­site-host inter­ac­tions or plant-herb­i­vore inter­ac­tions, the arms race between males and females over the con­trol of repro­duc­tion has been largely over­looked. Our recent work in Evol­u­tion Let­ters attempts to address this issue.

We focussed our efforts on under­stand­ing if females were cap­able of redu­cing last male sperm pre­ced­ence. We used the mod­el organ­ism Dro­so­phila melano­gaster, bet­ter known as the fruit fly. Not only are insects easy to work with and have a fast repro­duct­ive cycle mak­ing them ideal for such an exper­i­ments, but also inform­a­tion of female repro­duc­tion in this spe­cies would com­ple­ment a large body of know­ledge that already exists on the male traits doc­u­mented to evolve via sexu­al conflict.

Using molecu­lar clon­ing tech­niques estab­lished in the field, we developed male fruit flies that express either a green, red, or blue fluor­es­cent pro­tein on the head of their sperm. When females mate these males we can track the sperm with­in the repro­duct­ive tract and the patern­ity of the off­spring. We exposed females to these genet­ic­ally mod­i­fied males and recor­ded how many times females mated and with which male. We then com­pared the pat­terns of sperm stor­age as well as pat­terns of patern­ity to the pat­terns of mat­ing beha­viour. We found that females var­ied in the amount of both last male sperm pre­ced­ence and remat­ing rate. When we invest­ig­ated this vari­ation we found that the degree of last male sperm pre­ced­ence depended on the mat­ing rate of females: females that mated with more males and in quick suc­ces­sion showed a decrease in off­spring from the last male and con­sequently a more equally shared brood paternity.

From our exper­i­ments we find that females are not neces­sary defence­less when it comes to the tac­tics that males have developed to max­im­ize male repro­duct­ive suc­cess. Females can counter last male sperm pre­ced­ence by mod­u­lat­ing their mat­ing rate in order to max­im­ize the genet­ic diversity of their brood and ulti­mately their own per­son­al repro­duct­ive success.

 Our res­ults provide fur­ther evid­ence for a grow­ing body of work estab­lish­ing that females exert con­trol over their repro­duc­tion even after cop­u­la­tion – a cap­ab­il­ity pre­vi­ously reserved for males and sperm com­pet­i­tion. Work on sexu­al con­flict in this spe­cies allows us to fur­ther our under­stand­ing of not only the prin­ciples that gov­ern off­spring pro­duc­tion and sexu­al beha­viour but also identi­fy the mech­an­isms that make this beha­viour pos­sible. Although sexu­al rela­tion­ships will always be com­plic­ated, exper­i­ments like ours explore the factors that muddy the waters. One co-evol­u­tion­ary arms race at a time.

Dr Meghan Laturney is lead author on the study, which was car­ried out at the Uni­ver­sity of Gronin­gen. The paper is freely avail­able to read and down­load here.