Should females prefer old males?

A new study pub­lished in Evol­u­tion Let­ters invest­ig­ates wheth­er the bene­fits of mat­ing with an older, more exper­i­enced male out­weigh the costs that paternal sen­es­cence may con­fer to the off­spring. One of the study’s authors, Car­o­lina Segami, tells us more. 

Choos­ing a mate is a crit­ic­al decision in the lives of many anim­als. Females are often the choosi­est sex and spend much effort in select­ing a part­ner that can provide dir­ect bene­fits such as a suit­able ter­rit­ory and shared off­spring care, but also indir­ect bene­fits in the form of “good” genes that bene­fit her off­spring. But how can females pre­dict which male to choose to max­im­ise these bene­fits? There has been a long-last­ing debate on the use­ful­ness of select­ing an old male. On the one hand, old males are more exper­i­enced and should be able to provide bet­ter ter­rit­or­ies and care of the off­spring. Clearly, they sur­vived, mean­ing that they may also carry “good” genes that ensure sur­viv­al abil­it­ies that will be passed on to the off­spring. On the oth­er hand, old males may exper­i­ence sen­es­cence or age­ing.  This could mean that they could be less effi­cient than young­er males in secur­ing food and help­ing with the off­spring rear­ing. Anoth­er pos­sib­il­ity is that their sperm could be car­ry­ing more dele­ter­i­ous muta­tions. The out­come of this dilemma has been hard to test in wild sys­tems because detailed inform­a­tion from sev­er­al gen­er­a­tions is needed, and it is hard to dis­tin­guish between the dir­ect and indir­ect (genet­ic) benefits.

Collared flycatch­er Ficedula albicol­lis. Cred­it: Car­o­lina Segami

We used 18 years of data from a collared flycatch­er pop­u­la­tion in Sweden mon­itored by the Qvarn­ström lab to test wheth­er females should prefer old males.  Collared flycatch­ers must travel thou­sands of kilo­met­ers from south-Saha­ran Africa to forests in the north­ern with the goal of arriv­ing to their breed­ing grounds and get a shot at repro­du­cing. After that tir­ing jour­ney, females dir­ectly choose a suit­able male part­ner to breed with and the plumage traits of the males reveal their age. We found that females paired with older males indeed had more off­spring that suc­cess­fully fledged from the nest and returned to breed them­selves in con­sec­ut­ive years. This res­ult was mainly explained by young (1‑year old) males under­per­form­ing as mates. To test wheth­er these young males are gen­er­ally are worse mates because they lack suit­able exper­i­ence or because they have been exposed to a short­er peri­od of selec­tion, we used our long-term data to travel back in time. More pre­cisely, we com­pared the per­form­ance of males that sur­vived until older age with those who died young. To our sur­prise, we found that males who sur­vived until older age, were already per­form­ing well dur­ing their first year of breed­ing. There­fore, select­ive remov­al of low-qual­ity indi­vidu­als after year one, rather than gained exper­i­ence with age, explains why females in gen­er­al should avoid pair­ing with young males.

To dis­en­tangle dir­ect and genet­ic bene­fits, we used nat­ur­ally occur­ring extra-pair off­spring in nests of males of known age. Because collared flycatch­ers often engage in extra pair cop­u­la­tions, is not rare to find mixed broods sired by dif­fer­ent males. By com­par­ing with­in (sired by the male tak­ing care of the nest) and extra-pair off­spring (sired by anoth­er male) raised in the same nest-envir­on­ment, we were able to isol­ate the genet­ic effects of the bio­lo­gic­al fath­er (only exper­i­enced by off­spring sired by him) from the dir­ect effects that are shared by all nest­lings in the nest. We found that while with­in-pair off­spring out­per­form their extra-pair half-sib­lings when their fath­er is young (1 and 2 years old) the oppos­ite is true when their fath­er is old. This res­ult implies a neg­at­ive genet­ic effect of paternal age in their off­spring indic­at­ing sen­es­cence in the germline. To our know­ledge this is the first study to dis­en­tangle genet­ic from dir­ect paternal age effects in a wild sys­tem. 

So, should females prefer old males? Accord­ing to our res­ults, they should care­fully avoid first-year breed­ing males as social mates and acquire a part­ner that has been exposed to selec­tion for a longer peri­od. This is because old collared flycatch­er males provide super­i­or ter­rit­or­ies and paternal care (i.e., bet­ter envir­on­ment­al con­di­tions dur­ing off­spring growth). How­ever, in the best-case scen­ario, while form­ing a pair with an old male, her off­spring should ideally be sired by a rather young extra-pair male to avoid the genet­ic cost of mat­ing with an old male that has exper­i­enced germline senescence! 

The study’s lead author, Car­o­lina Segami, in the field. Cred­it: Lily Hilgers

Car­o­lina Segami is a PhD stu­dent in the Qvarn­ström lab, Depart­ment of Eco­logy & Genet­ics, Uppsala Uni­ver­sity. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Letters.