Evolution of maternal effect senescence
Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 2; pp. 362 - 367 |
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Main Authors | , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
12.01.2016
National Acad Sciences |
Subjects | |
Online Access | Get full text |
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Abstract | Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton’s evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton’s age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species. |
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AbstractList | Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton's evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton's age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species. Evolutionary theory underpins our understanding of the aging process. The many aspects of reproduction that decline with maternal age in animals include number of offspring born, offspring size, and neonatal survival. Current theories of aging ignore potential differences in the evolutionary pressures on these traits. Here, we combine two important branches of evolutionary theory to allow consideration of age-dependent selection at both offspring and maternal levels. We show that we should actually expect the rates of age-related decline in female fertility and offspring performance to diverge under selection. Our model has the potential to significantly improve our understanding of the evolution of reproductive senescence and, more generally, the variability of aging patterns in nature. Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton’s evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton’s age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species. Significance Evolutionary theory underpins our understanding of the aging process. The many aspects of reproduction that decline with maternal age in animals include number of offspring born, offspring size, and neonatal survival. Current theories of aging ignore potential differences in the evolutionary pressures on these traits. Here, we combine two important branches of evolutionary theory to allow consideration of age-dependent selection at both offspring and maternal levels. We show that we should actually expect the rates of age-related decline in female fertility and offspring performance to diverge under selection. Our model has the potential to significantly improve our understanding of the evolution of reproductive senescence and, more generally, the variability of aging patterns in nature. Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton’s evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton’s age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species. |
Author | Nussey, Daniel H. Moorad, Jacob A. |
Author_xml | – sequence: 1 givenname: Jacob A. surname: Moorad fullname: Moorad, Jacob A. – sequence: 2 givenname: Daniel H. surname: Nussey fullname: Nussey, Daniel H. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26715745$$D View this record in MEDLINE/PubMed |
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Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Jan 12, 2016 |
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Keywords | aging selection demography social indirect genetic effects |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: J.A.M. and D.H.N. designed research, performed research, and wrote the paper. Edited by James W. Vaupel, Max Planck Institute for Demographic Research, Rostock, Germany, and approved December 4, 2015 (received for review October 23, 2015) |
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Snippet | Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans).... Significance Evolutionary theory underpins our understanding of the aging process. The many aspects of reproduction that decline with maternal age in animals... Evolutionary theory underpins our understanding of the aging process. The many aspects of reproduction that decline with maternal age in animals include number... |
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SubjectTerms | Aging - physiology Animals Biological Evolution Biological Sciences Demographics Evolution Female Fertility Humans Maternal Age Mutation - genetics Population genetics Selection, Genetic |
Title | Evolution of maternal effect senescence |
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