Age-associated variation in reproduction and consequences of mating strategies in male house sparrows, Passer domesticus

Abstract

Sexual selection is a strong evolutionary force shaping the traits determining individual reproductive success. Such traits can be crucial for reproductive success before or after copulation (pre- versus post-copulatory sexual selection). However, little is known about how primary and secondary sexual traits vary in relation to male age in socially monogamous but genetically promiscuous (i.e. extra-pair) species. This is a particularly pressing question because extra-pair sires are more often older rather than younger males, which suggests that male age reflects genetic quality to females. Yet, older males are senescent males and produce lower quality offspring. Thus, females should actually avoid mating with older males. Furthermore, it is assumed that males that mate with multiple females achieve fitness benefits (higher lifetime reproductive success) compared to males that mate monogamously. This assumption underlies sexual selection theory. Additionally, it provides a straightforward explanation of why males in socially monogamous species engage in extra-pair mating: it maximises their reproductive success. Surprisingly, this classic claim has not been thoroughly quantified and thus awaits validation.In this thesis, I examined age-related variation in reproduction. Particularly, I studied how male age relates to mating strategies, sperm traits and reproductive success. I further quantified the fitness consequences of a males mating promiscuously over males mating monogamously. My study species was the house sparrow, Passer domesticus, a predominantly socially monogamous species. I studied captive and wild sparrows, both of exact known ages. Avian studies commonly rely on discriminating between first-year and older breeders only. Such a dichotomous discrimination of age prohibits analyses at all life history stages. Further, I quantified the lifetime reproductive success of wild sparrows. Knowledge of lifetime reproductive success is crucial for understanding, for instance, the fitness consequences of mating decisions.Extra-pair sires are commonly older males. It has been hypothesized that this is the result of older males having a pre-copulatory advantage over younger males. Chapter 2 put this hypothesis to the test and shows that male age seems unrelated to pre-copulatory male competition. Further, females did not base their pre-copulatory mate choice on male age, which refutes the idea of male age signalling genetic quality to females. Instead, postcopulatory mechanisms seem to underlie the pattern of extra-pair sires being older males.One of such post-copulatory mechanisms is sperm competition where sperm of multiple males compete for fertilisation of a female’s eggs. In birds, sperm can be sampled with relative ease and it is assumed that applying different methods of sperm collection does not affect sperm measurements. Chapter 3 experimentally tested whether two common methods of sperm collection indeed do not affect sperm measurements. Contrasting the previous assumption, sperm length varied according to sperm collection method. Thus, the practice of mixing sperm collection methods should be avoided or, at least, statistically controlled for.Chapter 4 followed up on the hypothesis that post-copulatory mechanisms might explain why extra-pair sires are often older males. The results showed that sperm morphology and indices of relative testes size seemed to be unaffected by male age. Yet, when considering the number of sperm that reached the egg of females, older males delivered more sperm than younger males. Hence, older males might have a post-copulatory competitive advantage over younger males.Chapter 5 answers the fundamental question of whether extra-pair paternity maximises male fitness. Surprisingly, the field of evolutionary ecology lacks empirical data supporting this classic claim. The results reveal that a promiscuous male mating strategy does not maximise male fitness, which contrasts expectations from sexual selection theory and calls for reconsidering the validity of this basic assumption.With this thesis, I thus contributed to clarifying the factors underlying the relationship between extra-pair paternity and male age. In sum, I found that older males have higher extrapair paternity not because of pre-copulatory male competition or female choice but probably because of a post-copulatory advantage. I also updated the current protocol of avian sperm sampling and advocated a standardised method to enhance comparability across and within studies. Finally, I quantified the fitness consequences of extra-pair paternity and discovered that it does not maximise male fitness.