Perspectives on mating system evolution

An introduction to Target Review Perspectives on mating–system evolution: comparing concepts in plants and animals (Clo et al. 2025)
by Matthew Hartfield

Our Tar­get Review paper “Per­spect­ives on mat­ing sys­tem evol­u­tion: com­par­ing con­cepts in plants and anim­als” has just been pub­lished in JEB. We are very excited to see this paper in print, giv­en it was a huge group effort that took a few years and many meet­ings for it to come together!

This paper ori­gin­ated at the ESEB meet­ing in Prague in 2022. Two of the authors – Jos­selin Clo and Mat­thew Hart­field – organ­ised a sym­posi­um there on “The Evol­u­tion­ary Eco­logy of Mat­ing Sys­tems”. The study of mat­ing sys­tems (“who mates with whom, and how often in a sexu­ally repro­du­cing pop­u­la­tion”) is a key research area in evol­u­tion­ary bio­logy, and one that we thought would gath­er a lot of atten­tion from the evol­u­tion com­munity. We received many strong applic­a­tions show­cas­ing the latest research, but one thing caught our attention.

Social­ising in Prague after the sym­posi­um! Photo cred­it: Mat­thew Hartfield.

Based on our own research, both of us ten­ded to think of ‘Mat­ing Sys­tems’ in terms of the evol­u­tion of self-fer­til­isa­tion, where indi­vidu­als are herm­aph­rod­ites that can fer­til­ise them­selves. Yet we also received many talks cov­er­ing mat­ing sys­tems in bipar­ent­al spe­cies, which covered the evol­u­tion of mate-pair form­a­tion (for example, are indi­vidu­als mono­gam­ous that form a single mat­ing pair at a time, or instead mate with mul­tiple indi­vidu­als?). These talks ten­ded to cov­er sim­il­ar themes, such as the effects of inbreed­ing and how indi­vidu­als inter­act in space, but the two research areas seemed to be dis­con­nec­ted from one anoth­er. We wanted to write a review paper cov­er­ing the sym­posi­um, and this seemed like an intriguing angle to con­sider for it.

A highly-self­ing plant, Ara­bidop­sis thali­ana (left) and the social spiders Ste­godyphus saras­inor­um (right). The evol­u­tion of both types of spe­cies has been invest­ig­ated through the lens of ‘mat­ing-sys­tem’ the­ory, but in dif­fer­ent ways. Photo cred­its: Wiki­pe­dia com­mons; Vir­gin­ia Sette­pani and Trine Bilde.

We assembled five oth­er attendees of the sym­posi­um to write the review. The brief was: is there a reas­on why the two main fields of mat­ing-sys­tem research (the evol­u­tion of self-fer­til­isa­tion, and mate-pair form­a­tion) have developed sep­ar­ately, and are there any them­at­ic over­laps that become appar­ent once we com­pare the two? This seem­ingly simple task led to plenty of dis­cus­sion over sev­er­al years (we were all busy with our day jobs!) in try­ing to work out what areas were truly over­lap­ping, and why the two research fields have developed sep­ar­ately. It didn’t help that each sub­field was huge, so try­ing to nar­row each of them down to their key ele­ments was a daunt­ing task in itself!

In the end, we focussed the com­par­is­on on the fol­low­ing five areas:

  • Advant­ages of inbreed­ing: This includes the trans­mis­sion advant­age of an allele for self-fer­til­isa­tion; an increase in kin selec­tion among spe­cies that inbreed; and vari­ous mech­an­isms of repro­duct­ive assurance.
  • Costs of inbreed­ing: The obvi­ous one is inbreed­ing depres­sion, which is rel­ev­ant to both self-fer­til­isa­tion and bipar­ent­al mat­ing. Yet there can also be a cost due to the lim­it­a­tion of inbred mat­ings; to give one example, there are a lack of male gam­etes as most were instead used for out­cross­ing or non-kin matings.
  • Mech­an­isms of inbreed­ing: In (self­ing) plants, this can include geitono­gamy (trans­fer of pol­len between flowers in the same indi­vidu­al) or delayed self­ing, arising only after out­cross­ing oppor­tun­it­ies have fin­ished. The­or­et­ic­ally, bipar­ent­al spe­cies can act­ively seek mates to increase inclus­ive fit­ness, but it is thought that the neg­at­ive effects of inbreed­ing counter this advantage.
  • Inbreed­ing avoid­ance: Includ­ing mech­an­isms such as self-incom­pat­ib­il­ity sys­tems, flor­al mor­pho­logy to pre­vent inbreed­ing, and pre-mat­ing dis­pers­al in animals.
  • Spa­tial dynam­ics: That is, how the dis­tri­bu­tion of indi­vidu­als, pol­lin­at­ors, and resources in space affect the evol­u­tion of mat­ing systems.

This com­par­is­on leads to the fol­low­ing pro­pos­als on how we can bet­ter com­pare the two fields of mat­ing-sys­tem research, to work towards a uni­fied study of this clas­sic research field:

  • Devel­op­ing nov­el the­ory that describes evol­u­tion­ary mech­an­isms, while expli­citly con­sid­er­ing dif­fer­ent types of mat­ing systems.
  • Bet­ter quan­ti­fic­a­tion of exist­ing con­cepts (e.g., the trans­mis­sion advant­age of self-fer­til­isa­tion), as even with­in each sub­field there are the­or­et­ic­al con­cepts with sur­pris­ingly little meas­ure­ment to them.
  • Is self-fer­til­isa­tion adapt­ive, or tol­er­ated? Inbreed­ing is usu­ally seen as dele­ter­i­ous in bipar­en­tial spe­cies when it arises. So does that mean that some highly-self­ing spe­cies do so due to loc­al cir­cum­stances, rather than because it is act­ively favoured?
  • Empir­ic­al tests and nov­el the­ory of how spa­tial feed­backs affect mat­ing-sys­tem evolution.

Our goal with this review is to make research­ers from each sub­field think more deeply about wheth­er con­cepts from oth­er mat­ing-sys­tem stud­ies would be rel­ev­ant to their own stud­ies, and use them accord­ingly. We hope you enjoy our work and that it’ll stim­u­late some nov­el ideas for future stud­ies in this excit­ing research area.

Related Posts