Dataset Information

Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants.

ABSTRACT: The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early-life over late-life reproduction. Studies on natural vertebrate populations show early reproduction may impair later-life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early-life reproduction and female age-specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age-specific fecundity and offspring survival, but significantly impaired a female's own later-life survival. Despite the negative effects of early reproduction on late-life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade-off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later-life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi-)captive breeding programmes of this endangered species.

SUBMITTER: Hayward AD

PROVIDER: S-EPMC4237172 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants.

Hayward A D AD Mar K U KU Lahdenperä M M Lummaa V V

Journal of evolutionary biology 20140303 4

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early-life over late-life reproduction. Studies on natural vertebrate populations show early reproduction may impair later-life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian eleph ...[more]

PMID: 24580655

Similar Datasets

Project description:BackgroundDemonstrating the impact that parents have on the fitness of their children is a crucial step towards understanding how parental investment has affected human evolution. Parents not only transfer genes to their children, they also influence their environments. By analyzing reproductive patterns within and between different categories of close relatives, this study provides insight into the genetic and environmental effects that parents have on the fitness of their offspring.MethodsWe use data spanning over two centuries from an exceptionally accurate Icelandic genealogy, Íslendingabók, to analyze the relationship between the fertility rates of close relatives. Also, using genetic data, we determine narrow sense heritability estimates (h2) to further explore the genetic impact on lifetime reproductive success. Finally, we construct four simulations to model the expected contribution of genes and resources on reproductive success.ResultsThe relationship between the reproduction of all full sibling pairs was significant and positive across all birth decades (r = 0.19) while the reproductive relationship between parents and offspring was often negative across many decades and undetectable overall (r = 0.00) (Fig. 1 and Table 1). Meanwhile, genetic data among 8,456 pairs of full siblings revealed a narrow sense heritability estimate (h2) of 0.00 for lifetime reproductive success. A resources model (following the rule that resources are transmitted from parents to children, distributed equally among siblings, and are the only factor affecting reproductive success) revealed a similar trend: a negative relationship between parent and offspring reproduction (r = - 0.35) but a positive relationship among full siblings (r = 0.28). The relationship between parent and offspring lifetime reproductive success (LRS) and full sibling LRS was strongly and positively correlated across time (r = 0.799, p < 0.001). Similarly, the LRS among full siblings was positively correlated with both the LRS among half siblings (r = 0.532, p = 0.011) and the relationship between the LRS of aunts and uncles with their nieces and nephews (r = 0.438, p = 0.042).DiscussionWe show that an individual's lifetime reproductive success is best predicted by the reproduction of their full and half siblings, but not their parents, grandparents or aunts and uncles. Because all siblings share at least one parent, we believe parental investment has had an important impact on fitness. Overall, these results indicate that direct parental investment, but not genes, is likely to have had an important and persistent impact on lifetime reproductive success across more than two centuries of Icelandic history.

Project description:IntroductionShort post-reproductive lifespan is widespread across species, but prolonged post-reproductive life-stages of potential adaptive significance have been reported only in few mammals with extreme longevity. Long post-reproductive lifespan contradicts classical evolutionary predictions of simultaneous senescence in survival and reproduction, and raises the question of whether extreme longevity in mammals promotes such a life-history. Among terrestrial mammals, elephants share the features with great apes and humans, of having long lifespan and offspring with long dependency. However, little data exists on the frequency of post-reproductive lifespan in elephants. Here we use extensive demographic records on semi-captive Asian elephants (n?=?1040) and genealogical data on pre-industrial women (n?=?5336) to provide the first comparisons of age-specific reproduction, survival and post-reproductive lifespan in both of these long-lived species.ResultsWe found that fertility decreased after age 50 in elephants, but the pattern differed from a total loss of fertility in menopausal women with many elephants continuing to reproduce at least until the age of 65 years. The probability of entering a non-reproductive state increased steadily in elephants from the earliest age of reproduction until age 65, with the longer living elephants continuing to reproduce until older ages, in contrast to humans whose termination probability increased rapidly after age 35 and reached 1 at 56 years, but did not depend on longevity. Post-reproductive lifespan reached 11-17 years in elephants and 26-27 years in humans living until old age (depending on method), but whereas half of human adult lifespan (of those reproductive females surviving to the age of 5% fecundity) was spent as post-reproductive, only one eighth was in elephants. Consequently, although some elephants have long post-reproductive lifespans, relatively few individuals reach such a phase and the decline in fertility generally parallels declines in survivorship in contrast to humans with a decoupling of senescence in somatic and reproductive functions.ConclusionsOur results show that the reproductive and survival patterns of Asian elephants differ from other long-lived animals exhibiting menopause, such as humans, and extreme longevity alone does not promote the evolution of menopause or post-reproductive lifespan, adding weight to the unusual kin-selected benefits suggested to favour such traits in humans and killer whales.

Dataset Information

Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants.

Publications

Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets