Sexy sons and greenbeards

In our latest author blog, Gonçalo Faria explains how his new paper in Evol­u­tion Let­ters invest­ig­ates the con­nec­tions between two clas­sic ideas in evol­u­tion­ary bio­logy: the “sexy son hypo­thes­is” and the “green­beard effect”.

Two major the­or­ies dom­in­ate con­tem­por­ary evol­u­tion­ary bio­logy: sexu­al selec­tion, which con­cerns how nat­ur­al selec­tion can work through dif­fer­ences in mat­ing suc­cess; and kin selec­tion, which con­cerns how nat­ur­al selec­tion can work through the repro­duct­ive suc­cess of an individual’s genet­ic rel­at­ives. Both the­or­ies made their first appear­ance in Charles Darwin’s The Ori­gin of Spe­cies, and have sub­sequently developed into enorm­ous lit­er­at­ures – with sur­pris­ingly little cross-talk between them.

Dar­win went onto greatly devel­op the the­ory of sexu­al selec­tion in his massive tome The Des­cent of Man, and Selec­tion in Rela­tion to Sex. An early cham­pi­on of this the­ory was R. A. Fish­er, who sug­ges­ted what is now known as the “sexy son hypo­thes­is”. Accord­ing to this idea, females will be favoured to pref­er­en­tially mate with males who exhib­it con­spicu­ous orna­ment­a­tion if oth­er females already hap­pen to find this orna­ment­a­tion attract­ive because, by mat­ing with orna­men­ted males, females will be more likely to have orna­men­ted sons, who will be more attract­ive to poten­tial mat­ing partners.

Build­ing upon Darwin’s ini­tial mus­ings that kin selec­tion could explain the adapt­a­tions of sterile work­ers in insect soci­et­ies, Hamilton developed these ideas into a gen­er­al math­em­at­ic­al the­ory of how nat­ur­al selec­tion works both through the indi­vidu­al’s own repro­duc­tion and that of its rel­at­ives. In doing so, he pro­posed what is now known by the “green­beard effect” – this col­our­ful name being coined by Richard Dawkins in The Selfish Gene – to explain how altru­ist­ic beha­viours could evolve in absence of gene­a­lo­gic­al related­ness. The idea assents on two genes being present. One of the genes causes a dis­play of a con­spicu­ous mark­er, such as a green beard. The oth­er gene cause its car­ri­ers to act altru­ist­ic­ally toward indi­vidu­als car­ry­ing a green beard. If the two genes tend to be asso­ci­ated with­in the same indi­vidu­als, then the altru­ist­ic beha­viour can be favoured by nat­ur­al selec­tion because it is ulti­mately help­ing cop­ies of itself.

My paper, co-authored with my PhD super­visors, Susana Varela and Andy Gard­ner, con­cerns the idea that the sexy-son effect is a kind of green­beard effect. Spe­cific­ally, if females vary in their pref­er­ence, and males in their orna­ment­a­tion, then the res­ult­ing assort­at­ive mat­ing of choosy females with orna­men­ted males ensures that the alleles under­pin­ning female pref­er­ence and male orna­ment­a­tion will tend to be present in the same indi­vidu­als. There­fore, when a female car­ri­er of the pref­er­ence allele mates with an orna­men­ted male, she is likely provid­ing a fit­ness bene­fit to a car­ri­er of the same allele. This appear to be equi­val­ent to the green­beard effect, where car­ri­ers of the altru­ist­ic allele provide a fit­ness bene­fit to green bearded indi­vidu­als, likely car­ry­ing the same altru­ist­ic allele. This pos­sib­il­ity had been dis­cussed by Dawkins in The Blind Watch­maker and later by Gard­ner, in a paper co-authored with Tom­maso Piz­zari, but had not been explored form­ally. If this is cor­rect, then it should be pos­sible to integ­rate the con­cepts and approaches of those two dif­fer­ent effects and that is the object­ive of our work. We do this in four dif­fer­ent parts.

First, we ask what kind of green­beard effect is involved in the sexy-son effect. In the green­beard effect lit­er­at­ure, four broad cat­egor­ies can be used to clas­si­fy green­beard effects: fac­ultat­ive-help­ing green­beards, where green­beards enact help­ing beha­viour toward fel­low green­beards but not toward non-green­beards; fac­ultat­ive-harm­ing green­beards, where indi­vidu­als enact harm­ing beha­viour towards non-green­beards but not towards fel­low green­beards; oblig­ate-help­ing green­beards enact help­ing beha­viour toward all social part­ners, but only fel­low green­beards are able to bene­fit from this; and oblig­ate-harm­ing green­beards enact harm­ing beha­viour toward all social part­ners, but only non-green­beards are vul­ner­able to its dele­ter­i­ous effects. It turns out that those same cat­egor­ies can be used to dis­tin­guish four dif­fer­ent types of sexy-son effects, depend­ing on how female pref­er­ence is being enacted and its effect upon orna­men­ted and non-orna­men­ted males.

Second, we invest­ig­ate if the sexy-son effect is also vul­ner­able to what is known, in the green­beard lit­er­at­ure, as the prob­lem of “false­beards”. False­beards are those indi­vidu­als who cheat by grow­ing a beard but without enact­ing any altru­ism. Piz­zari and Gard­ner sug­ges­ted that the sexy-son effect may involve a kind of green­beard effect that is rel­at­ively res­ist­ant to false­beards. Spe­cific­ally, the pres­ence of assort­at­ive mat­ing may con­tinu­ally build up the asso­ci­ation between the two traits, pre­vent­ing the break­down of the effect through the evol­u­tion of false­beards. Incor­por­at­ing assort­at­ive mat­ing into a green­beard effect mod­el, how­ever, does not pre­vent the prob­lem of false­beards and, in fact, the sexy-son effect suf­fers from an equi­val­ent prob­lem, known in the lit­er­at­ure as the lek para­dox, whereby female pref­er­ence makes itself redund­ant by elim­in­at­ing the very genet­ic vari­ation that defines pre­ferred versus non-pre­ferred males.

Might, then, the solu­tion that have been iden­ti­fied for the lek para­dox have applic­a­tion in the prob­lem of false­beards? This is the third ques­tion of our work. One well-known way to pre­vent the lek para­dox is to con­tinu­ally fuel vari­ation into the male orna­ment locus, such that female pref­er­ence does not become redund­ant. We find that simply intro­du­cing mutants does not help, but it does sta­bil­ize the green­beard effect if assort­at­ive mat­ing is also present. This high­lights the sim­il­ar­it­ies between the prob­lem of false­beards and the lek para­dox and, con­sequently, the sim­il­ar­ity between the green­beard effect and the sexy-son effect.

Lastly, both green­beard and sexy-son effects have dif­fi­culties to get off the ground. Spe­cific­ally, they both require a high fre­quency of dis­crim­in­at­ory beha­viour to be already present in the pop­u­la­tion before the effects them­selves start being favoured by nat­ur­al selec­tion. Gard­ner, in an art­icle writ­ten with Stu­art West, showed that pop­u­la­tion struc­ture can help the estab­lish­ment of the green­beard effect in the pop­u­la­tion because loc­al social inter­ac­tions allow the fre­quency of green­beard indi­vidu­als to be loc­ally high enough to be favoured, even if they are glob­ally rare. Our final con­tri­bu­tion is to show that pop­u­la­tion struc­ture is also a pos­sible solu­tion to help sexy-son effects to evolve from rarity.

This works illus­trates how, if a con­cep­tu­al bridge can be built between two dif­fer­ent top­ics, old res­ults can lead to new insights in unex­pec­ted places.

Gonçalo Faria is a PhD stu­dent at the School of Bio­logy, Uni­ver­sity of St. Andrews. The full paper is freely avail­able to read and down­load from Evol­u­tion let­ters here.