Selecting on age of female reproduction affects lifespan in both sexes and age-dependent reproductive effort in female (but not male) Ceratitis cosyra

Abstract

The trade-off between lifespan and reproduction is central to our understanding of life-history evolution. Laboratory selection experiments have been a powerful tool for quantifying this trade-off, but these tend to be restricted in taxonomic scope, which may limit our understanding. In addition, research often focuses on the trade-off between lifespan and reproductive effort in females, and far less data test how lifespan trades off with different aspects of male reproduction (e.g. pre- and post-copulatory reproductive investment). Here, we examined the trade-off between lifespan and reproduction in females and males of the marula fruit fly, Ceratitis cosyra (Walker) (Diptera: Tephritidae). To do so, we selected downward or upward on age of peak female egg laying in C. cosyra for twenty generations. In multiple generations, we measured female and male lifespan and body size, female daily and lifetime fecundity, male courtship and mating success, as well as the number of sperm transferred at different ages and sperm storage asymmetry in spermathecae. Our selection regime appeared to achieve its aim; egg laying peaked earlier in females from downward selected lines than upward selected lines. The number of sperm transferred by males decreased in the upward selected flies, but other male reproductive traits remained the same across selection regimes. In contrast, with the wider literature, upward selection did not extend the lifespan of females or males after ten generations of selection. While lifespan in both sexes responded to selection on female egg laying schedules, it did not do so in a straightforward way. Moreover, male investment in reproductive traits was largely independent of selection regime. These counter-intuitive findings highlight the importance of working with a broad range of species and of considering the trade-off between reproduction and lifespan in both sexes.

Significance statement

The trade-off between lifespan and reproduction has been extensively studied in model species using various types of laboratory selection. A limited number of species have been considered using this approach, and the majority of the studies have focused on female, rather than male, reproductive effort. Here, we selected downwards and upwards on age of female reproduction in the marula fruit fly and measured survival, female fecundity, reproductive schedule, as well as male sperm transfer, sperm storage asymmetry, mating and calling success. We found a moderate trade-off between lifespan and early fecundity in downward selected flies, whereas no obvious trade-off was observed in upward selected lines. Regardless of the selection regime, reproductive scheduling was affected in females but not in males, while lifespan was affected in both sexes. Our results show that the timing of reproduction can evolve independently across the sexes, highlighting the importance of studying both females and males.