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The role of menopause and reproductive senescence in a long-lived social mammal

BACKGROUND: Menopause is a seemingly maladaptive life-history trait that is found in many long-lived mammals. There are two competing evolutionary hypotheses for this phenomenon; in the adaptive view of menopause, the cessation of reproduction may increase the fitness of older females; in the non-ad...

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Autores principales: Ward, Eric J, Parsons, Kim, Holmes, Elizabeth E, Balcomb, Ken C, Ford, John KB
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2644688/
https://www.ncbi.nlm.nih.gov/pubmed/19192288
http://dx.doi.org/10.1186/1742-9994-6-4
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author Ward, Eric J
Parsons, Kim
Holmes, Elizabeth E
Balcomb, Ken C
Ford, John KB
author_facet Ward, Eric J
Parsons, Kim
Holmes, Elizabeth E
Balcomb, Ken C
Ford, John KB
author_sort Ward, Eric J
collection PubMed
description BACKGROUND: Menopause is a seemingly maladaptive life-history trait that is found in many long-lived mammals. There are two competing evolutionary hypotheses for this phenomenon; in the adaptive view of menopause, the cessation of reproduction may increase the fitness of older females; in the non-adaptive view, menopause may be explained by physiological deterioration with age. The decline and eventual cessation of reproduction has been documented in a number of mammalian species, however the evolutionary cause of this trait is unknown. RESULTS: We examined a unique 30-year time series of killer whales, tracking the reproductive performance of individuals through time. Killer whales are extremely long-lived, and may have the longest documented post-reproductive lifespan of any mammal, including humans. We found no strong support for either of the adaptive hypotheses of menopause; there was little support for the presence of post-reproductive females benefitting their daughter's reproductive performance (interbirth interval and reproductive lifespan of daughters), or the number of mature recruits to the population. Oldest mothers (> 35) did appear to have a small positive impact on calf survival, suggesting that females may gain experience with age. There was mixed support for the grandmother hypothesis – grandoffspring survival probabilities were not influenced by living grandmothers, but grandmothers may positively influence survival of juveniles at a critical life stage. CONCLUSION: Although existing data do not allow us to examine evolutionary tradeoffs between survival and reproduction for this species, we were able to examine the effect of maternal age on offspring survival. Our results are consistent with similar studies of other mammals – oldest mothers appear to be better mothers, producing calves with higher survival rates. Studies of juvenile survival in humans have reported positive benefits of grandmothers on newly weaned infants; our results indicate that 3-year old killer whales may experience a positive benefit from helpful grandmothers. While our research provides little support for menopause evolving to provide fitness benefits to mothers or grandmothers, our work supports previous research showing that menopause and long post-reproductive lifespans are not a human phenomenon.
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spelling pubmed-26446882009-02-19 The role of menopause and reproductive senescence in a long-lived social mammal Ward, Eric J Parsons, Kim Holmes, Elizabeth E Balcomb, Ken C Ford, John KB Front Zool Research BACKGROUND: Menopause is a seemingly maladaptive life-history trait that is found in many long-lived mammals. There are two competing evolutionary hypotheses for this phenomenon; in the adaptive view of menopause, the cessation of reproduction may increase the fitness of older females; in the non-adaptive view, menopause may be explained by physiological deterioration with age. The decline and eventual cessation of reproduction has been documented in a number of mammalian species, however the evolutionary cause of this trait is unknown. RESULTS: We examined a unique 30-year time series of killer whales, tracking the reproductive performance of individuals through time. Killer whales are extremely long-lived, and may have the longest documented post-reproductive lifespan of any mammal, including humans. We found no strong support for either of the adaptive hypotheses of menopause; there was little support for the presence of post-reproductive females benefitting their daughter's reproductive performance (interbirth interval and reproductive lifespan of daughters), or the number of mature recruits to the population. Oldest mothers (> 35) did appear to have a small positive impact on calf survival, suggesting that females may gain experience with age. There was mixed support for the grandmother hypothesis – grandoffspring survival probabilities were not influenced by living grandmothers, but grandmothers may positively influence survival of juveniles at a critical life stage. CONCLUSION: Although existing data do not allow us to examine evolutionary tradeoffs between survival and reproduction for this species, we were able to examine the effect of maternal age on offspring survival. Our results are consistent with similar studies of other mammals – oldest mothers appear to be better mothers, producing calves with higher survival rates. Studies of juvenile survival in humans have reported positive benefits of grandmothers on newly weaned infants; our results indicate that 3-year old killer whales may experience a positive benefit from helpful grandmothers. While our research provides little support for menopause evolving to provide fitness benefits to mothers or grandmothers, our work supports previous research showing that menopause and long post-reproductive lifespans are not a human phenomenon. BioMed Central 2009-02-03 /pmc/articles/PMC2644688/ /pubmed/19192288 http://dx.doi.org/10.1186/1742-9994-6-4 Text en Copyright © 2009 Ward et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Ward, Eric J
Parsons, Kim
Holmes, Elizabeth E
Balcomb, Ken C
Ford, John KB
The role of menopause and reproductive senescence in a long-lived social mammal
title The role of menopause and reproductive senescence in a long-lived social mammal
title_full The role of menopause and reproductive senescence in a long-lived social mammal
title_fullStr The role of menopause and reproductive senescence in a long-lived social mammal
title_full_unstemmed The role of menopause and reproductive senescence in a long-lived social mammal
title_short The role of menopause and reproductive senescence in a long-lived social mammal
title_sort role of menopause and reproductive senescence in a long-lived social mammal
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2644688/
https://www.ncbi.nlm.nih.gov/pubmed/19192288
http://dx.doi.org/10.1186/1742-9994-6-4
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