Population spatial structure moderates sexual conflict

A new study pub­lished in Evol­u­tion Let­ters uses an exper­i­ment­al evol­u­tion approach to provide import­ant new insights into how sexu­al inter­ac­tions are mod­u­lated. Author Dr Fran­cisco Gar­cia-Gonza­lez tells us more.

Dur­ing the times of Justini­an the Great, around the year 550 A.D., the legend says that a ruler in a vast region of what was known as His­pan­ia estab­lished a harsh decree affect­ing the cit­ies con­tained in his realm: in some cit­ies mono­gamy was imposed and mar­riages were to be arranged and enforced to take place between indi­vidu­als who did not have the chance to select their part­ner. In the remain­ing cit­ies, poly­gamy was allowed in such a way that men and women could choose their part­ners freely and could repro­duce with dif­fer­ent part­ners. In these poly­gam­ous pop­u­la­tions com­pet­i­tion among men for access to females and female mate choice was fierce. The ruler fur­ther dic­tated that half of the cit­ies in each of the two groups were to be sub­divided into dif­fer­ent sec­tions, while the oth­er half were to remain undi­vided. Thus, there were four dif­fer­ent groups of pop­u­la­tions: undi­vided mono­gam­ous, divided mono­gam­ous, undi­vided poly­gam­ous and divided poly­gam­ous. The final rule stated that the decree had to be in place for over a thou­sand years.

The sexu­al selec­tion decree. Four pop­u­la­tions were undi­vided mono­gam­ous (blue circles), anoth­er four divided mono­gam­ous (red circles), anoth­er four undi­vided poly­gam­ous (blue squares) and the remain­ing four pop­u­la­tions were divided poly­gam­ous (red squares).

The above legend is false, of course, but ima­gine that it was true and now, in the 21st cen­tury and after over 40 gen­er­a­tions of dif­fer­ent select­ive pres­sures in those pop­u­la­tions, we could answer ques­tions such as: Are the indi­vidu­als in the dif­fer­ent cit­ies dif­fer­ent in any way? Has a his­tory of relaxed or intense sexu­al selec­tion and/or pop­u­la­tion sub­di­vi­sion shaped mor­pho­lo­gic­al, physiolo­gic­al or beha­vi­our­al traits in males and females? Have these dif­fer­ent his­tor­ies related to sexu­al selec­tion intens­ity affected the viab­il­ity of populations? 

These are some of the ques­tions that we are address­ing in our lab using a humble but use­ful and inter­est­ing study sys­tem, Cal­lo­sobruchus mac­u­lat­us, a pest beetle of stored legumes that is pop­u­lar in stud­ies of the evol­u­tion­ary eco­logy of sexu­al selec­tion and sexu­al con­flict. In par­tic­u­lar, in our latest study in Evol­u­tion Let­ters we focused on wheth­er selec­tion his­tory asso­ci­ated to mat­ing sys­tem (monogamy/polygamy) and the pres­ence or absence of pop­u­la­tion sub­di­vi­sion and con­nectiv­ity (known as meta­pop­u­la­tion struc­ture) mod­u­lated sexu­al con­flict dynam­ics. Sexu­al con­flict occurs when the interests of males and females over mat­ing and repro­duc­tion (or par­ent­al care in some spe­cies) dif­fer. In recent dec­ades it has become obvi­ous that this con­flict of interest between the sexes is wide­spread in the anim­al king­dom, from insects to humans, and that it has far-reach­ing evol­u­tion­ary implications.

Cal­lo­sobruchus mac­u­lat­us mat­ing pair. Photo: Eduardo Rodriguez-Exposito

So, using C. mac­u­lat­us, a spe­cies endowed with some of the best examples of sexu­al con­flict traits, includ­ing a remark­able spiny intro­mit­tent organ in the male gen­italia that dam­ages the female repro­duct­ive tract dur­ing cop­u­la­tion, we did some­thing sim­il­ar to the made-up legend above. Why did we do it? Not simply because we could, but because this kind of exper­i­ment­al evol­u­tion can provide import­ant insights into the drivers and mod­u­lat­ors of sexu­al inter­ac­tions. In a study span­ning over 40 gen­er­a­tions under the con­di­tions described above (enforced mono­gamy vs free poly­gamy added to the pres­ence or absence of pop­u­la­tion sub­di­vi­sion and migra­tion among sub­pop­u­la­tions), we ran sev­er­al assays to inspect the con­sequences of mat­ing. We did this by mat­ing stand­ard test­er indi­vidu­als from out­side the selec­tion exper­i­ment to indi­vidu­als from the dif­fer­ent exper­i­ment­al pop­u­la­tions (undi­vided mono­gam­ous, divided mono­gam­ous, undi­vided poly­gam­ous and divided poly­gam­ous), and check­ing longev­ity and repro­duct­ive suc­cess trajectories.

Most research on the evol­u­tion of sexu­al con­flict has been con­duc­ted using simple pop­u­la­tion scen­ari­os (for instance, in the absence of pop­u­la­tion spa­tial struc­ture), or uni­form envir­on­ments, but our study chal­lenged these tra­di­tion­al empir­ic­al under­tak­ings. What made our study unique is that we addi­tion­ally imposed selec­tion arising from meta­pop­u­la­tion structure.

The res­ults of this study, co-authored by Eduardo Rodrig­uez-Exposito, sup­port tra­di­tion­al sexu­al con­flict the­ory by show­ing that females from pop­u­la­tions with a his­tory of intense sexu­al selec­tion and sexu­al con­flict evolve high­er res­ist­ance to male harm, and that enforced mono­gamy leads to the evol­u­tion of less res­ist­ant females. How­ever, our study uncovered that this pat­tern of ant­ag­on­ist­ic coe­volu­tion between the sexes is reversed in spa­tially struc­tured pop­u­la­tions. These find­ings indic­ate that the eco­lo­gic­al and demo­graph­ic con­text mod­er­ates the con­sequences of sexu­al antagonism. 

This dis­cov­ery has import­ant implic­a­tions for aspects of sexu­al selec­tion, pop­u­la­tion dynam­ics, con­ser­va­tion bio­logy and pest con­trol. We hope our study will spur fur­ther the­or­et­ic­al and empir­ic­al research focus­ing on the inter­play between eco­logy and evol­u­tion in defin­ing male-female interactions.

Dr Fran­cisco (Paco) Gar­cia-Gonza­lez is a Seni­or Research Sci­ent­ist at Doñana Bio­lo­gic­al Sta­tion-CSIC (Span­ish Research Coun­cil) and an Adjunct Research Fel­low at the Centre for Evol­u­tion­ary Bio­logy (The Uni­ver­sity of West­ern Aus­tralia). The ori­gin­al art­icle is freely avail­able to read and down­load from Evol­u­tion Letters.