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Sex, long life and the evolutionary transition to cooperative breeding in birds.

ABSTRACT: Long life is a typical feature of individuals living in cooperative societies. One explanation is that group living lowers mortality, which selects for longer life. Alternatively, long life may make the evolution of cooperation more likely by ensuring a long breeding tenure, making helping behaviour and queuing for breeding positions worthwhile. The benefit of queuing will, however, depend on whether individuals gain indirect fitness benefits while helping, which is determined by female promiscuity. Where promiscuity is high and therefore the indirect fitness benefits of helping are low, cooperation can still be favoured by an even longer life span. We present the results of comparative analyses designed to test the likelihood of a causal relationship between longevity and cooperative breeding by reconstructing ancestral states of cooperative breeding across birds, and by examining the effect of female promiscuity on the relationship between these two traits. We found that long life makes the evolution of cooperation more likely and that promiscuous cooperative species are exceptionally long lived. These results make sense of promiscuity in cooperative breeders and clarify the importance of life-history traits in the evolution of cooperative breeding, illustrating that cooperation can evolve via the combination of indirect and direct fitness benefits.

SUBMITTER: Downing PA

PROVIDER: S-EPMC4614776 | biostudies-literature | 2015 Oct

REPOSITORIES: biostudies-literature

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Sex, long life and the evolutionary transition to cooperative breeding in birds.

Downing Philip A PA Cornwallis Charlie K CK Griffin Ashleigh S AS

Proceedings. Biological sciences 20151001 1816

Long life is a typical feature of individuals living in cooperative societies. One explanation is that group living lowers mortality, which selects for longer life. Alternatively, long life may make the evolution of cooperation more likely by ensuring a long breeding tenure, making helping behaviour and queuing for breeding positions worthwhile. The benefit of queuing will, however, depend on whether individuals gain indirect fitness benefits while helping, which is determined by female promiscu ...[more]

PMID: 26400743

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Project description:Cooperative breeding is a form of breeding system where in addition to a core breeding pair, one or more usually non-breeding individuals provide offspring care. Cooperative breeding is widespread in birds, but its origin and maintenance in contemporary populations are debated. Although deviations in adult sex ratio (ASR, the proportion of males in the adult population) have been hypothesized to influence the occurrence of cooperative breeding because of the resulting surplus of one sex and limited availability of breeding partners, this hypothesis has not been tested across a wide range of taxa. By using data from 188 bird species and phylogenetically controlled analyses, we show that cooperatively breeding species have more male-biased ASRs than non-cooperative species. Importantly, ASR predicts helper sex ratio: in species with more male-biased ASR, helper sex ratio is also more male biased. We also show that offspring sex ratios do not predict ASRs, so that the skewed ASRs emerge during the period when individuals aim to obtain a breeding position or later during adulthood. In line with this result, we found that ASR (among both cooperatively and non-cooperatively breeding species) is inversely related to sex bias in dispersal distance, suggesting that the cost of dispersal is more severe for the further-dispersing sex. As females usually disperse further in birds, this explains the generally male-biased ASR, and in combination with benefits of philopatry for males, this probably explains why ASR is more biased in cooperatively breeding species. Taken together, our results suggest that a sex bias in helping in cooperatively breeding species relates to biased ASRs. We propose that this relationship is driven by sex-specific costs and benefits of dispersal and helping, as well as other demographic factors. Future phylogenetic comparative and experimental work is needed to establish how this relationship emerges.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Project description:The most studied comparison of aging and maximum lifespan potential (MLSP) among endotherms involves the 7-fold longevity difference between rats (MLSP 5y) and pigeons (MLSP 35y). A widely accepted theory explaining MLSP differences between species is the oxidative stress theory, which purports that reactive oxygen species (ROS) produced during mitochondrial respiration damage bio-molecules and eventually lead to the breakdown of regulatory systems and consequent death. Previous rat-pigeon studies compared only aspects of the oxidative stress theory and most concluded that the lower mitochondrial superoxide production of pigeons compared to rats was responsible for their much greater longevity. This conclusion is based mainly on data from one tissue (the heart) using one mitochondrial substrate (succinate). Studies on heart mitochondria using pyruvate as a mitochondrial substrate gave contradictory results. We believe the conclusion that birds produce less mitochondrial superoxide than mammals is unwarranted. We have revisited the rat-pigeon comparison in the most comprehensive manner to date. We have measured superoxide production (by heart, skeletal muscle and liver mitochondria), five different antioxidants in plasma, three tissues and mitochondria, membrane fatty acid composition (in seven tissues and three mitochondria), and biomarkers of oxidative damage. The only substantial and consistent difference that we have observed between rats and pigeons is their membrane fatty acid composition, with rats having membranes that are more susceptible to damage. This suggests that, although there was no difference in superoxide production, there is likely a much greater production of lipid-based ROS in the rat. We conclude that the differences in superoxide production reported previously were due to the arbitrary selection of heart muscle to source mitochondria and the provision of succinate. Had mitochondria been harvested from other tissues or other relevant mitochondrial metabolic substrates been used, then very different conclusions regarding differences in oxidative stress would have been reached.

Dataset Information

Sex, long life and the evolutionary transition to cooperative breeding in birds.

Publications

Sex, long life and the evolutionary transition to cooperative breeding in birds.

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