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 ( 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.
Multiple mating by females is common and often driven by social constraints on female mate choice. However, females mate with multiple males even in systems without these social constraints and rates of multiple mating tend to be highly variable within and between populations. In lek mating systems, females are able to assess multiple males and their choice is unrestricted by pair bonds or the need for biparental care, yet some females mate with multiple males. To better understand the factors affecting variation in multiple mating, we investigated the occurrence of multiple paternity within clutches in a highly polygynous lek mating system. Using long‐term data on genetic paternity, survival, social status and individual age from a population of lance‐tailed manakins We found that inexperienced males, including new alphas and rare beta sires, were disproportionately likely to share paternity when they sired any chicks. In contrast, female age (experience) was unrelated to multiple paternity. Multiple mating did not result in higher reproductive success or reduced variance in success for females, and there were neither consistently promiscuous females nor males that consistently shared paternity. The occurrence of multiple paternity in this lek mating system was best explained by female choice related to male characteristics that change with male experience. Our results support the hypothesis that there is a developmental component to the occurrence of multiple mating, and suggest females choose to mate multiply when their choices are not optimal.
- NSF-PAR ID:
- 10458090
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 89
- Issue:
- 5
- ISSN:
- 0021-8790
- Page Range / eLocation ID:
- p. 1142-1152
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract 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. -
more » « less
Abstract The social and mating systems of orangutans, one of our closest relatives, remain poorly understood. Orangutans (
Pongo spp. ) are highly sexually dimorphic and females are philopatric and maintain individual, but overlapping home ranges, whereas males disperse, are non-territorial and wide-ranging, and show bimaturism, with many years between reaching sexual maturity and attaining full secondary sexual characteristics (including cheek pads (flanges) and emitting long calls). We report on 21 assigned paternities, among 35 flanged and 15 unflanged, genotyped male Bornean orangutans (Pongo pygmaeus wurmbii ), studied from 2003 to 2018 in Tuanan (Central Kalimantan, Indonesia). All 10 infants born since mid-2003 with an already identified sire were sired by flanged males. All adult males ranged well beyond the study area (c. 1000 ha), and their dominance relations fluctuated even within short periods. However, 5 of the 10 identified sires had multiple offspring within the monitored area. Several sired over a period of c. 10 years, which overlapped with siring periods of other males. The long-calling behavior of sires indicated they were not consistently dominant over other males in the area around the time of known conceptions. Instead, when they were seen in the area, the known sires spent most of their time within the home ranges of the females whose offspring they sired. Overall, successful sires were older and more often resident than others.Significance statement It is difficult to assess reproductive success for individuals of long-lived species, especially for dispersing males, who cannot be monitored throughout their lives. Due to extremely long interbirth intervals, orangutans have highly male-skewed operational sex ratios and thus intensive male-male competition for every conception. Paternity analyses matched 21 immature Bornean orangutans with their most likely sire (only 10 of 50 genotyped males) in a natural population. Half of these identified sires had multiple offspring in the study area spread over periods of at least 10 years, despite frequently ranging outside this area. Dominance was a poor predictor of success, but, consistent with female mating tactics to reduce the risk of infanticide, known “sires” tended to have relatively high local presence, which seems to contribute to the males’ siring success. The results highlight the importance of large protected areas to enable a natural pattern of dispersal and ranging.
-
more » « less
Abstract Background Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we hypothesize that in polygamous species these roles change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis by assessing fitness costs and benefits of multiple matings in both males and females in a polygamous moth species, as in moths not males but females are the signalers and males are the responders.
Results We found that multiple matings confer fitness costs and benefits for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but only 67% of the males and 14% of the females mated successfully in all five nights. In addition, the female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, more than 3 matings decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings.
Conclusion Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.
-
more » « less
In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (
Lemur catta ) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wildL. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in differentL. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity forL. catta males. -
more » « less
Abstract Intraspecific variation in animal mating systems can have important implications for ecological, evolutionary and demographic processes in wild populations. For example, patterns of mating can impact social structure, dispersal, effective population size and inbreeding. However, few species have been studied in sufficient detail to elucidate mating system plasticity and its dependence on ecological and demographic factors. Southern elephant seals (
Mirounga leonina ) have long been regarded as a textbook example of a polygynous mating system, with dominant ‘beachmaster’ males controlling harems of up to several hundred females. However, behavioural and genetic studies have uncovered appreciable geographic variation in the strength of polygyny among elephant seal populations. We, therefore, used molecular parentage analysis to investigate patterns of parentage in a small satellite colony of elephant seals at the South Shetland Islands. We hypothesised that dominant males would be able to successfully monopolise the relatively small numbers of females present in the colony, leading to relatively high levels of polygyny. A total of 424 individuals (comprising 33 adult males, 101 adult females and 290 pups) sampled over 8 years were genotyped at 20 microsatellites and reproductive success was analysed by genetically assigning parents. Paternity could only be assigned to 31 pups (10.7%), despite our panel of genetic markers being highly informative and the genotyping error rate being very low. The strength of inferred polygyny was weak in comparison to previous genetic studies of the same species, with the most successful male fathering only seven pups over the entire course of our study. Our results show that, even in a species long regarded as a model for extreme polygyny, male reproductive skew can vary substantially among populations.
