Sex‐specific patterns of senescence in Nazca boobies linked to mating system

Abstract

Under life‐history theories of ageing, increased senescence should follow relatively high reproductive effort. This expectation has rarely been tested against senescence varying between and within the two sexes, although such an approach may clarify the origins of sex‐specific ageing in the context of a given mating system. Nazca boobies (Sula granti; a seabird) practise serial monogamy and biparental care. A male‐biased population sex ratio results in earlier and more frequent breeding by females. Based on sex‐specific reproductive schedules, females were expected to show faster age‐related decline for survival and reproduction. Within each sex, high reproductive effort in early life was expected to reduce late‐life performance and accelerate senescence. Longitudinal data were used to (a) evaluate the sex specificity of reproductive and actuarial senescence and then (b) test for early‐/late‐life fitness trade‐offs within each sex. Within‐sex analyses inform an interpretation of sex differences in senescence based on costs of reproduction. Analyses incorporated individual heterogeneity in breeding performance and cohort‐level differences in early‐adult environments. Females showed marginally more intense actuarial senescence and stronger age‐related declines for fledging success. The opposite pattern (earlier and faster male senescence) was found for breeding probability. Individual reproductive effort in early life positively predicted late‐life reproductive performance in both sexes and thus did not support a causal link between early‐reproduction/late‐life fitness trade‐offs and sex differences in ageing. A high‐quality diet in early adulthood reduced late‐life survival (females) and accelerated senescence for fledging success (males). This study documents clear variation in ageing patterns—by sex, early‐adult environment and early‐adult reproductive effort—with implications for the role mating systems and early‐life environments play in determining ageing patterns. Absent evidence for a disposable soma mechanism, patterns of sex differences in senescence may result from age‐ and condition‐dependent mate choice interacting with this population's male‐biased sex ratio and mate rotation.

Sex‐independent senescence in a cooperatively breeding mammal

“…To test for sex differences in ageing patterns, we adopted a similar approach to Tompkins and Anderson () and fitted six models for each trait (Table S1). In model 1, age was included as a quadratic function, and males and females were assumed to follow the same age trajectory.…”

“…Yet, not all studies that have looked for sex differences in polygynous species have found them (Tidière et al, 2014(Tidière et al, , 2015Toïgo & Gaillard, 2003), and more generally, the evidence for a direct role of sexual selection on rates of ageing is equivocal (Bonduriansky, Maklakov, Zajitschek, & Brooks, 2008;Graves, 2007;Maklakov, Bonduriansky, & Brooks, 2009). This is likely because males and females can compete in different ways, the traits involved can entail different costs, and might also be expressed at different stages of lifespan (Clutton-Brock, 1983;Ralls & Mesnick, 2009;Stockley & Bro-Jørgensen, 2011;Tompkins & Anderson, 2019). In this context, it is important to appreciate that sex differences in survival rates and senescence depend on the characteristics of the two sexes which, in turn, depend on the specific selection pressures generated by intraspecific competition in the two sexes rather than on sex differences in reproductive variance (Clutton-Brock, 1983).…”

Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort

“…Recent correlative evidence suggests that population structure, such as sex-ratio, affects individual reproductive effort with potential sex-specific consequences on senescence [34,35]. In particular, variation in sex-ratio is predicted to modulate the cost of mating, through the strength of sexual selection in males [36], influencing the putative trade-off between reproductive effort and somatic maintenance [11].…”

Egg size variation in the context of polyandry: a case study using long-term field data from snowy plovers

“…Hence, in polygynous species, strong sexual selection and intrasexual competition are thought to accelerate senescence and may lead to high mortality rates in males (Clutton-Brock & Isvaran, 2007;Bonduriansky et al, 2008;Maklakov & Lummaa, 2013;Greiner et al, 2014;Beirne et al, 2015;Tidière et al, 2015; but see Lemaître et al, 2020). Conversely, in monogamous species where sexual selection is not as intense, senescence acts similarly on both males and females (Clutton-Brock & Isvaran, 2007) or shows only moderate biases towards either sex (e.g., Lecomte et al, 2010;Froy et al, 2017;Tompkins & Anderson, 2019). If sexual selection leads to high senescence one should expect to detect senescence among females in sex-rolereversed species -yet, senescence of females in sex-role-reversed species has remained understudied.…”