Does sexual selection help or hinder population performance?

A new study pub­lished today in Evol­u­tion Let­ters shows that pop­u­la­tions with an evol­u­tion­ary his­tory of strong sexu­al selec­tion are able to invade com­pet­it­or pop­u­la­tions more rap­idly. Here, lead author Dr Joanne God­win tells us more.

Costs: sexu­al selec­tion vs. nat­ur­al selection

No dis­cus­sion of sexu­al selec­tion is com­plete without the clichéd pic­ture of a pea­cock. Pea­cocks even fea­tured in Darwin’s ori­gin­al think­ing on the mech­an­isms of evol­u­tion, caus­ing him to write that ‘the sight of a feath­er in a peacock’s tail, whenev­er I gaze at it, makes me sick’, due to their appar­ent lack of sur­viv­al value. Pea­cock feath­ers exem­pli­fy extra­vag­ant sex-spe­cif­ic traits which, although ener­get­ic­ally costly and some­times with neg­at­ive impacts on sur­viv­al, evolve due to the advant­age they provide for mat­ing and repro­duct­ive success.

Icon­ic sexu­ally selec­ted traits also include antlers and horns used in both com­pet­i­tion between rivals and as a sig­nal for mate choice. How­ever, it has been sug­ges­ted that the vast antlers of the Irish Elk may have been so costly that it pushed the spe­cies over an ‘extinc­tion threshold’. The bal­ance between invest­ing in repro­duc­tion or sur­viv­al is thus a del­ic­ate one and while we under­stand many of the costs and bene­fits of sexu­al selec­tion for indi­vidu­als, how this impacts at the pop­u­la­tion level remains unclear.

Bene­fits: heightened con­di­tion and reduced muta­tion load

While pea­cock feath­ers may have caused Dar­win some dis­quiet, he also describes how ‘sexu­al selec­tion will give its aid to ordin­ary selec­tion, by assur­ing to the most vig­or­ous and best adap­ted males the greatest num­ber of off­spring’, sug­gest­ing that, rather than work­ing in oppos­i­tion, these evol­u­tion­ary forces could or should work along­side each other.

The elab­or­ate and costly nature of many sexu­ally selec­ted traits means their devel­op­ment and main­ten­ance is often depend­ent on the ‘con­di­tion’ of an indi­vidu­al – the pool of resources avail­able to alloc­ate to traits. The great­er this pool of resources, the more can be alloc­ated not only to bright­er feath­ers or lar­ger antlers, but also to devel­op­ment, growth, repair and fecund­ity. The great­er an individual’s con­di­tion, there­fore, the more likely they are to max­im­ise their evol­u­tion­ary fit­ness. Cru­cially, this means that any beha­vi­our­al, physiolo­gic­al or bio­chem­ic­al trait which allows an indi­vidu­al to increase their pool of resources, or to make more effi­cient use of them, will be favoured by sexu­al selec­tion as well as nat­ur­al selec­tion. Align­ment of sexu­al and nat­ur­al selec­tion for improved con­di­tion can there­fore cre­ate lin­eages and pop­u­la­tions with increased aver­age fitness.

In addi­tion, if sexu­al selec­tion act­ing via com­pet­i­tion between rivals and mate choice, ensures only those in highest con­di­tion gain the greatest share of repro­duct­ive suc­cess and con­trib­ute the most to the next gen­er­a­tion, this should increase the rate that bene­fi­cial alleles become fixed and aid the remov­al of dele­ter­i­ous muta­tion load. Fur­ther­more, the vari­ety of traits which can improve con­di­tion means these pro­cesses could occur across the whole gen­ome. Key papers by Agraw­al (2001) and Siller (2001), sug­gest the longer-term bene­fits to pop­u­la­tions of reduced muta­tion load across the gen­ome, could out­weigh the cost of pro­du­cing males and explain the main­ten­ance of sexu­al reproduction.

Inva­sion abil­ity: a hol­ist­ic test of fitness

Our new study tested the idea that an evol­u­tion­ary his­tory of sexu­al selec­tion can improve mean fit­ness with­in a pop­u­la­tion, com­pared to when it is removed. We used the abil­ity of indi­vidu­als from con­trast­ing sexu­al selec­tion back­grounds to invade into com­pet­it­or pop­u­la­tions across mul­tiple gen­er­a­tions as a hol­ist­ic meas­ure of over­all fit­ness. Inva­sion suc­cess will depend on a wide range of traits in both sexes and a com­pet­it­ive advant­age across life stages and gen­er­a­tions, there­fore incor­por­at­ing key fit­ness com­pon­ents of viab­il­ity, fecund­ity and hap­loid selec­tion in addi­tion to mat­ing and fer­til­isa­tion success.

We made use of exper­i­ment­ally evolved pop­u­la­tions of the red flour beetle, Tri­bol­i­um castaneum, hav­ing exper­i­enced 77 gen­er­a­tions of con­trast­ing strengths of sexu­al selec­tion under either mono­gam­ous or poly­androus mat­ing sys­tems dur­ing the adult life stage. With­in these pop­u­la­tions and at every gen­er­a­tion, adults are placed in either poly­androus groups (1 female and 5 males) cre­at­ing oppor­tun­it­ies for com­pet­i­tion between rivals and choice of mates (SS+), or mono­gam­ous pairs (1 female and 1 male) which removes com­pet­i­tion and choice (SS-).

Males from these sexu­al selec­tion back­grounds were intro­duced into small pop­u­la­tions of a nov­el com­pet­it­or strain, known as ‘Reindeer’ due to their dis­tinct­ive swollen anten­nae, which allowed us to mon­it­or the spread of the wild-type phen­o­type dis­played by the invaders. Hav­ing col­on­ised the lar­ger Reindeer com­pet­it­or pop­u­la­tions with a hand­ful of males from strong or weak sexu­al selec­tion back­grounds, we tracked inva­sion across the fol­low­ing 8 gen­er­a­tions, meas­ur­ing any genet­ic spread linked to the mark­er phenotypes.

Our res­ults show that where indi­vidu­als have an evol­u­tion­ary his­tory of poly­andry (red), they are able to invade more rap­idly and com­pletely than those with a his­tory of mono­gamy (blue). At the end of the year-long inva­sion exper­i­ment, invaders from high­er sexu­al selec­tion back­grounds had almost com­pletely elim­in­ated the ori­gin­al com­pet­it­or pop­u­la­tion back­ground. To under­stand what par­tic­u­lar advant­ages are gained under stronger sexu­al selec­tion, we fol­lowed this up with assays of fer­til­ity and pop­u­la­tion genet­ic sim­u­la­tions which sug­ges­ted that fit­ness is improved through the off­spring, as well as adult life stages, in both sexes.

Why does this matter?

Evid­ence that sexu­al selec­tion improves aver­age pop­u­la­tion fit­ness provides empir­ic­al sup­port for mod­els explain­ing how costly sexu­al repro­duc­tion can per­sist. Moreover, pop­u­la­tions are facing ever-increas­ing threats from hab­it­at loss and frag­ment­a­tion, over­ex­ploit­a­tion and envir­on­ment­al change. So, in addi­tion to the align­ment of nat­ur­al and sexu­al selec­tion being an inter­est­ing the­or­et­ic­al ques­tion, it will also have import­ant implic­a­tions for pop­u­la­tion viab­il­ity, extinc­tion risk and con­ser­va­tion planning.

Dr Joanne God­win is a post-doc­tor­al research­er at the Uni­ver­sity of East Anglia. The ori­gin­al study is freely avail­able to read and down­load here.