Evolutionary determinants of reproductive seasonality: a theoretical approach

Abstract

Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood for many species, in part due to a lacunary theoretical framework. Because seasonal cycles are increasingly disrupted by climate change, a better understanding of the ecology of reproductive seasonality could generate important insights on how climate change may affect biodiversity. The goal of this study was to investigate the drivers of evolutionary transitions towards reproductive seasonality using a realistic agent-based optimisation model simulating the life cycle of a female yellow baboon, who typically breeds year-round. Specifically, we tested the influence of three ecological traits (environmental seasonality, productivity and unpredictability) and three life-history traits (daily reproductive energy expenditure, reproductive cycle length and infant extrinsic mortality) on the intensity of reproductive seasonality. To do so, we simulated diverse reproductive phenology strategies (from non-seasonal to highly seasonal), assessed which were optimal and computed, for the set of optimal strategies, the intensity of reproductive seasonality. We then induced variation in each trait of interest and examined how it affected the intensity of reproductive seasonality. We found significant effects of all three environmental traits: high reproductive seasonality was favoured by high environmental seasonality, low environmental productivity and low unpredictability. It was further, and most strongly, favoured by high daily reproductive energy expenditure. In contrast, there was no significant effect of reproductive cycle length and infant extrinsic mortality. Our modelling approach successfully disentangled the effects of environmental seasonality, productivity and unpredictability on the intensity of reproductive seasonality, which likely all contribute to generate the well-known association between latitude and reproductive seasonality. Our results further highlight the critical importance of life history pace on the evolution of reproductive seasonality. Overall, this study contributes a powerful theoretical framework and modelling tool that may apply across the life-history space, as well as sheds new light on the emergence and maintenance of non-seasonal breeding in slow-living species, including humans.

Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictability

“…Two recent studies found no or little effect of climatic unpredictability on the intensity of reproductive seasonality at the population level, one in chacma baboons (Dezeure et al, 2023) and one on yellow baboons using a modelling approach (Burtschell et al, 2023), questioning the robustness of the effect found in this study. This discrepancy may come from the fact that unpredictable climates select for reproductive flexibility, rather than nonseasonal breeding.…”

“…While English et al (2012) found that higher inter-annual variation in food availability decreased the intensity of birth synchrony across 38 ungulate species, two studies of red deer, Cervus elaphus L. (Loe et al, 2005) and chacma baboons, Papio ursinus (Dezeure et al, 2023) found no effect of environmental unpredictability on reproductive seasonality. A recent modelling study similarly detected limited effects of environmental unpredictability on evolutionary transitions to nonseasonal breeding (Burtschell et al, 2023).…”

“…This discrepancy may come from the fact that unpredictable climates select for reproductive flexibility, rather than nonseasonal breeding. In fact, the study by Burtschell et al, 2023 revealed that increasing climatic unpredictability was associated with a lower variance, but not a lower mean, in the intensity of reproductive seasonality. In addition, the effect of climatic unpredictability may be better detected across space than time, i.e., by comparing different populations living in distinct climates and environments, as is the case here, than by comparing the same population across time, as was the case for Dezeure et al, 2023. Different study designs should be combined, across time, taxonomic or spatial scales, to reveal the full complexity of selective pressures at play.…”

“…Flexibility in reproductive phenology may be facilitated by several mechanisms. First, a slower life history may allow papionin species to spread the energetic costs of reproduction over a prolonged period, such that pregnant or lactating females face only a small daily extra energetic expenditure that can be afforded at any time, as suggested by a recent modelling study (Burtschell et al, 2023). In addition, unlike many other mammals, cercopithecids do not use strict photoperiodic cues to trigger their reproduction (Heldstab et al, 2020) but may instead exhibit condition-induced reproduction, whereby conceptions (and/or cycle resumption after lactation) are more likely to occur when females are in better condition (Alberts et al, 2005;Beehner, Onderdonk, Alberts, & Altmann, 2006).…”

“…Further, latitude covaries negatively with environmental productivity, i.e., overall food availability in a given environment. Variation in productivity may alter the benefits of seasonal breeding, as populations living in more productive habitats may face less pressure to breed seasonally (Burtschell et al, 2023).…”