Battle of the sexes resolved

A new paper pub­lished in Evol­u­tion Let­ters has shown how the evol­u­tion of gene expres­sion dif­fer­ences in males and females can lead to con­flict res­ol­u­tion between the sexes. We spoke to lead author Dr Alis­on Wright to find out more about her latest findings. 

EL: The idea of the “battle of the sexes” is famil­i­ar to most people, but can you explain why this con­flict exists in the first place?

Males and females in many anim­als have dis­tinct repro­duct­ive roles, interests and bio­logy. Evol­u­tion some­times works very dif­fer­ently between males and females, and can push the sexes in oppos­ite dir­ec­tions. Often, this can lead to sub­stan­tially dif­fer­ent phen­o­typ­ic optima between the sexes, a situ­ation referred to as sexu­al conflict.

Males and females share an almost identic­al set of genes and many traits are thought to be encoded by the same genes between the sexes. These shared genet­ic path­ways can pose sig­ni­fic­ant prob­lems when evol­u­tion acts dif­fer­ently on males and females, as very often the same gene has dif­fer­ent optim­al func­tions in either sex. This is called intra-locus sexu­al con­flict and is thought to be wide­spread across the entire gen­ome. In the­ory, unre­solved sexu­al con­flict in pop­u­la­tions could hinder the evol­u­tion of sex dif­fer­ences and there­fore incur neg­at­ive fit­ness con­sequences. How­ever, the under­ly­ing causes of sexu­al con­flict, and the poten­tial for it to be resolved, has been heav­ily debated.

EL: What first led you to ques­tion wheth­er the evol­u­tion of gene expres­sion dif­fer­ences between the sexes could alle­vi­ate some of this conflict?

Much of my work to date has focused on the evol­u­tion of the sex chro­mo­somes and the role that they play in gen­er­at­ing sex dif­fer­ences. Sex chro­mo­somes are the only region of the gen­ome that is shared unequally between the sexes and they are there­fore pre­dicted to har­bour genes import­ant for sexu­al dimorph­ism. For example, in mam­mals with XY chro­mo­somes, the Y is key to male repro­duc­tion and fer­til­ity. It is widely assumed that the form­a­tion of new sex chro­mo­somes can resolve sexu­al con­flict and recently we set out to test this the­ory using wild pop­u­la­tions of gup­pies. We found that sexu­al con­flict over col­our pro­motes the form­a­tion and diver­gence of sex chro­mo­somes, con­sist­ent with this long­stand­ing theory.

How­ever, sex chro­mo­somes con­tain only a few genes in many anim­als, as is the case in the guppy, or are absent entirely, as in many rep­tiles and fish where sex is determ­ined by the envir­on­ment. There­fore, sexu­al con­flict for auto­somal genes is assumed to occur through the evol­u­tion of gene expres­sion dif­fer­ences between females and males, ulti­mately lead­ing to phen­o­typ­ic dimorph­ism. Tran­scrip­tion­al dif­fer­ences can be quite pro­nounced between the sexes and our pre­vi­ous research has shown that rap­id turnover of sex biased expres­sion across a clade of birds is driv­en by sexu­al selec­tion as a res­ult of expres­sion changes in males. Recently, there has been con­sid­er­able debate about the poten­tial role of reg­u­lat­ory evol­u­tion to resolve sexu­al conflict.

We ori­gin­ally developed a set of cri­ter­ia to identi­fy groups of genes sub­ject to sexu­al con­flict with the aim to test the­or­et­ic­al pre­dic­tions about their dis­tri­bu­tion on the sex chro­mo­somes. How­ever, we quickly real­ised that this was a power­ful approach for shed­ding light on the debate sur­round­ing reg­u­lat­ory evol­u­tion and test fun­da­ment­al pre­dic­tions about the nature and res­ol­u­tion of sexu­al con­flict across the entire genome!

EL: You car­ried out your research on a fish spe­cies, the Trin­id­a­di­an guppy. How is sexu­al con­flict mani­fes­ted in these fish, and what makes them par­tic­u­larly well suited for test­ing your hypotheses?

Gup­pies are a clas­sic mod­el spe­cies for the study of sexu­al selec­tion, par­tic­u­larly regard­ing col­our and mate choice. Males are extremely col­our­ful and females prefer to mate with males with large areas of orange caroten­oid pig­ment­a­tion on their tail. How­ever, whilst orna­men­ted males have high­er repro­duct­ive suc­cess, they also attract more pred­at­ors in the wild. In con­trast, males do not prefer to mate with col­our­ful females and there­fore col­our­a­tion genes only increase pred­a­tion pres­sure when expressed in females. Addi­tion­ally, male col­our and female pref­er­ence for col­our­ful males var­ies with pred­a­tion regime in the wild.

These land­mark stud­ies of sexu­al con­flict over col­our in gup­pies, and the wealth of phen­o­typ­ic data, make gup­pies a fant­ast­ic mod­el in which to apply gen­om­ic tools to study the mani­fest­a­tion and res­ol­u­tion of sexu­al con­flict across the genome.

Sexu­al con­flict can res­ult from dif­fer­ent types of selec­tion pres­sures, includ­ing repro­duct­ive fit­ness and sur­viv­al. The guppy tail com­bines genes involved in male col­our­a­tion, which influ­ence repro­duc­tion, as well as skin dir­ectly inter­fa­cing with the envir­on­ment, which influ­ence pred­a­tion and sur­viv­al. Study­ing the guppy tail there­fore offers an excit­ing oppor­tun­ity to dis­tin­guish the dif­fer­ent scen­ari­os giv­ing rise to sexu­al con­flict. Fur­ther­more, that fact that gup­pies can be kept in the labor­at­ory makes it pos­sible to con­trol many demo­graph­ic pro­cesses which could con­found our gen­om­ic meas­ures of sexu­al con­flict in the wild.

EL: In your paper, you say that sexu­al con­flict leaves a “sig­na­ture” in the genet­ic make-up of a pop­u­la­tion. Can you explain what that means?

Yes, sexu­al con­flict leaves dis­tinct sig­na­tures in sequence data that we can use to under­stand the nature of sexu­al con­flict and how it is resolved. Intra-locus con­flict leads to dif­fer­ent ver­sions or ‘alleles’ of the same gene being favoured in males versus females, or vice versa. This can lead to bal­an­cing selec­tion, where mul­tiple ver­sions of the same gene are main­tained with­in the pop­u­la­tion. In turn, this res­ults in elev­ated genet­ic diversity which can be meas­ured using Tajima’s D. Tajima’s D is a pop­u­la­tion genet­ic test stat­ist­ic to con­trast pat­terns of genet­ic diversity to those expec­ted under neut­ral expectation.

How­ever, we can’t use pat­terns of elev­ated genet­ic diversity to dis­tin­guish between sexu­al con­flict arising over repro­duc­tion or con­flict over sur­viv­al. To do this, we stud­ied genet­ic dif­fer­ences between males and females using the pop­u­la­tion genet­ic meas­ure inter-sexu­al F_ST. Essen­tially, at the point of con­cep­tion, we expect dif­fer­ent ver­sions of the same gene to be identic­al between the sexes. How­ever, if an allele affects sur­viv­al or pred­a­tion dif­fer­ently between males and females, then this will be reflec­ted in genet­ic diver­gence between the sexes in adulthood.

We essen­tially com­bined these two sig­na­tures of sexu­al con­flict to under­stand why sexu­al con­flict arises and how it can be resolved.

EL: What were the key find­ings of your study, and what do you per­son­ally think is the most excit­ing discovery?

We found that the major­ity of sexu­al con­flict is pro­duced through con­flict­ing selec­tion over repro­duct­ive interests of males and females, and that sexu­al con­flict has the poten­tial to main­tain genet­ic diversity through bal­an­cing selec­tion. This could explain why pat­terns of genet­ic vari­ation are much great­er in many anim­als than might be expected.

We also showed that reg­u­lat­ory evol­u­tion, the evol­u­tion of gene expres­sion dif­fer­ences between males and females, is a rap­id and effi­cient route to resolv­ing sexu­al con­flict. This res­ult is very excit­ing as we find that sex-biased expres­sion decouples male and female phen­o­types, lead­ing to the evol­u­tion of sep­ar­ate sex-spe­cif­ic archi­tec­tures where alleles have phen­o­typ­ic effects in one sex but not the other.

EL: What is the import­ance of these find­ings for our under­stand­ing of how the genet­ic basis of dif­fer­ent char­ac­ter­ist­ics can vary and evolve?

Genet­ic cor­rel­a­tions between males and females arising from shar­ing a gen­ome are widely assumed to hinder the evol­u­tion of sexu­al dimorph­ism and adapt­a­tion more gen­er­ally. Our res­ults sug­gest that the con­straints imposed by shar­ing a gen­ome might not be so dif­fi­cult to over­come and that the evol­u­tion of new genet­ic archi­tec­tures are more labile than pre­vi­ously thought. It is also becom­ing increas­ingly appar­ent that sexu­al con­flict can shape broad pat­terns of genet­ic diversity across the entire gen­ome. Genet­ic vari­ation is the source of evol­u­tion­ary change, and there­fore sexu­al con­flict could pro­mote rap­id adapt­a­tion and evolvability.

EL: What do you think are the most inter­est­ing unanswered ques­tions in this field going forward?

This study raises a num­ber of really excit­ing ques­tions I am keen to pur­sue fur­ther. I am par­tic­u­larly inter­ested in study­ing sexu­al con­flict in a com­par­at­ive frame­work to under­stand the turnover of sexu­al con­flict and speed at which it can be resolved. How quickly can male and female phen­o­types be decoupled? Does this depend on the nature of sexu­al con­flict and con­flict­ing selec­tion pres­sures? Does sex-link­age pro­mote faster con­flict res­ol­u­tion? How does this impact the strength of bal­an­cing selection?

Dr Alis­on Wright is a NERC Inde­pend­ent Research Fel­low at the Depart­ment of Anim­al & Plant Sci­ences, Uni­ver­sity of Shef­field. Find out more about her research here.