Effects of mating age and mate age on lifespan and reproduction in a horned beetle

Abstract

Mating young can cause early death due to resulting energetic depletion, physical damage, or sexually transmitted disease, whereas waiting too long to mate has the risks of suffering reproductive senescence or death before finding a mate. The ideal age for reproducing also depends on the mate’s age, as young partners may be more aggressive or less fertile and experienced than mature partners. Therefore, longevity and lifetime reproductive success depend on the combination rather than the individual effects of self- and the mate’s mating age, but this idea has not been formally explored. Here I evaluated lifetime reproductive success and longevity in males and females mated at different ages (i.e., young or mature) with mates of the same or a different age. As a study system, I used the horned dung beetle Euoniticellus intermedius, a classic study subject with intense sexual selection for male horn size, which is a reliable indicator of male strength and condition. For both males and females, mating young severely reduced lifespan, independent of the mate’s age, body, or male horn size. Due to reduced survival, females, but not males, had fewer offspring, with a stronger fitness effect suffered by mature than by young females. Regarding reproductive success, mature males and females had 3.4 and 1.6 times more offspring, respectively, when mated with mature than when mated with young partners, independently of their own body and horn sizes. Reproductive success of young males or females was not sensitive to the mate’s age. These results indicate that the optimal onset of reproduction and the ideal reproductive investment are highly dependent on the combination of self- and the mate’s age.

Significance statement

A very important decision in life is when to mate for the first time. Whereas mating too young can be risky or suboptimal, waiting too long increases the chance of dying before finding a mate. Here I show that in dung beetles, it can be equally important to choose the correct mate’s age in order to maximize lifetime reproduction. The most dramatic decision is for individuals (mainly males) that take a long time to mate, whose fitness get reduced by up to three times when mated with young rather than mature couples. This idea had never been tested in animals, and dung beetles showed that a combination of self- and the mate’s age will be determinant of how much progeny can animals have and how deadly it can be to take maladaptive decisions.