Breeding seasonality generates reproductive trade-offs in a long-lived mammal

Abstract

The evolutionary benefits of reproductive seasonality are usually measured by a single fitness component, namely offspring survival to nutritional independence (Bronson, 2009). Yet different fitness components may be maximised by dissimilar birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons (Papio ursinus) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. Like humans, baboons are eclectic omnivores, give birth every 1-3 years to a single offspring that develops slowly, and typically breed year-round. We identify two distinct optimal birth timings in the annual cycle, located 4-months apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother-offspring conflict (Maestripieri, 2002). Maternal trade-offs over birth timing, which extend into mother-offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Such trade-offs may substantially weaken the benefits of seasonal reproduction, and our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans. SIGNIFICANCE STATEMENTWhy some species breed seasonally and others do not remain unclear. The fitness consequences of birth timing have traditionally been measured on offspring survival, ignoring other fitness components. We investigated the effects of birth timing on two fitness components in wild baboons, who breed year-round despite living in a seasonal savannah. Birth timing generates a trade-off between offspring survival and future maternal reproductive pace, meaning that mothers cannot maximize both. When birth timing favours maternal reproductive pace (instead of offspring survival), behavioural manifestations of mother-offspring conflict around weaning are intense. These results open new avenues to understand the evolution of reproductive timings in long-lived animals including humans, where such reproductive trade-offs may commonly weaken the intensity of reproductive seasonality.