Life span and reproductive cost explain interspecific variation in the optimal onset of reproduction

Mourocq, Emeline; Bize, Pierre; Bouwhuis, Sandra; Bradley, Russell W.; Charmantier, Anne; Solis, Carlos; Drobniak, Szymon M.; Espie, Richard H. M.; Herényi, Márton; Hötker, Hermann; Krüger, Oliver; Marzluff, John M.; Møller, Anders Pape; Nakagawa, Shinichi; Phillips, Richard A.; Radford, Andrew N.; Roulin, Alexandre; Török, János; Valencia, Juliana; Pol, Martijn van de; Warkentin, Ian G.; Winney, Isabel; Wood, Andrew G.; Griesser, Michael

doi:10.1111/evo.12853

Cited by 33 publications

(52 citation statements)

References 73 publications

(164 reference statements)

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“…Our results strengthen the importance of taking into account age and sex when studying life histories, even among monogamous species in which both sexes exhibit similar parental care1291129. Based on a unique long-term monitoring of know-age marked individuals in a population of a territorial vulture, we found that sex asymmetries constrained the age of recruitment and the local survival of breeding individuals, but not breeding success.…”

Section: Discussionsupporting

confidence: 76%

“…Differences in age-dependent demographic parameters between sexes are also common in nature1011, especially among species showing intense competition for mates (polygynous species)1012, and/or body-sized dimorphic species with asymmetric parental roles13. However, sex-specific life-histories exist even in monogamous species with low sexual body-size dimorphism and similar parental investment in reproduction911.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

“…However, sex-specific life-histories exist even in monogamous species with low sexual body-size dimorphism and similar parental investment in reproduction911. For example, recruitment (i.e., age of first breeding) differs between sexes in several bird species, including long-lived raptors111415. In addition, sex-specific costs of reproduction1617, susceptibility to human-related mortality1819 or to diseases and parasites20 may be responsible for sex-biased survival.…”

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confidence: 99%

“…Existing demographic studies have focused on the description of basic parameters, with few studies addressing the combined contribution of age and sex2425, which are essential for a robust diagnosis of population dynamics and a better understanding of life histories evolution1112. In fact, among long-lived territorial species it is very difficult to achieve large sample sizes of known-age marked birds for long time periods (as that obtained for short lived and/or colonial species)11, which precludes an examination of how aging affects individual life-history strategies. For this reason, potential sex-specific trade-offs between recruitment, breeding success and/or survival remain understudied26.…”

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confidence: 99%

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Sex- and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger

Sanz‐Aguilar

Cortés‐Avizanda

Serrano

et al. 2017

Sci Rep

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In long-lived species, the age-, stage- and/or sex-dependent patterns of survival and reproduction determine the evolution of life history strategies, the shape of the reproductive value, and ultimately population dynamics. We evaluate the combined effects of age and sex in recruitment, breeder survival and breeding success of the globally endangered Egyptian vulture (Neophron percnopterus), using 31-years of exhaustive data on marked individuals in Spain. Mean age of first reproduction was 7-yrs for both sexes, but females showed an earlier median and a larger variance than males. We found an age-related improvement in breeding success at the population level responding to the selective appearance and disappearance of phenotypes of different quality but unrelated to within-individual aging effects. Old males (≥8 yrs) showed a higher survival than both young males (≤7 yrs) and females, these later in turn not showing aging effects. Evolutionary trade-offs between age of recruitment and fitness (probably related to costs of territory acquisition and defense) as well as human-related mortality may explain these findings. Sex- and age-related differences in foraging strategies and susceptibility to toxics could be behind the relatively low survival of females and young males, adding a new concern for the conservation of this endangered species.

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Section: Discussionsupporting

confidence: 76%

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confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Sex- and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger

Sanz‐Aguilar

Cortés‐Avizanda

Serrano

et al. 2017

Sci Rep

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Blood testosterone levels in sickness and in health: Male chimpanzee testosterone levels decrease in face of an immune challenge

Sonnweber

Stevens

Hohmann

et al. 2021

American J Primatol

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As an integral part of the immune response, testosterone secretion is inhibited when an individual is confronted with an immune challenge. Testosterone‐mediated physiological, morphological, and behavioral traits are compromised at times of impaired health. Nevertheless, males of some species seem to maintain high levels of testosterone when confronted with an immune challenge, upholding competitive strength but compromising their immune response. It has been argued that this phenomenon will occur only in species living in social systems with high degrees of male‐male competition over mating opportunities. Male chimpanzees contest over access to fertile females and dominants sire the majority of offspring. This male mating pattern makes chimpanzees a candidate species where we could expect males to maintain high testosterone levels, compromising their immune response, to ensure immediate reproductive success. We measured blood testosterone levels in male and female chimpanzees, who expressed clinical symptoms (symptomatic) or showed no evidence of clinical disease on assessment (asymptomatic). For females, we expected to find lower testosterone levels in symptomatic individuals than in asymptomatic subjects. In males, we would predict lower testosterone levels in symptomatic individuals than in asymptomatic males, if the immune response leads to a decrease in testosterone secretion. Alternatively, males could have equal levels of testosterone when symptomatic and asymptomatic, upholding competitive strength. Our results show that male chimpanzees exhibit lower levels of testosterone when confronted with an immune challenge than when being asymptomatic. This suggests that male testosterone secretion is suppressed as part of the immune response, which potentially increases survival and lifetime reproductive success. It will, however, negatively impact momentary competitive ability. Also, males may employ different mating strategies, some of which are less testosterone‐driven (e.g., affiliative strategies). Consequently, in some individuals, the costs of maintaining high testosterone levels may not outweigh the potential gain in reproductive success.

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Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories

Authier

Aubry

Cam

2017

Ecology and Evolution

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Understanding the processes behind change in reproductive state along life‐history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life‐history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population‐level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade‐off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life‐history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.

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Life span and reproductive cost explain interspecific variation in the optimal onset of reproduction

Cited by 33 publications

References 73 publications

Sex- and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger

Sex- and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger

Blood testosterone levels in sickness and in health: Male chimpanzee testosterone levels decrease in face of an immune challenge

Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories

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