The observed pattern and hidden process of female reproductive trajectories across the life span in a non‐human primate

Age‐specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross‐sectional data, where senescence especially late in life can be confounded by se...

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Veröffentlicht in:The Journal of animal ecology 2021-12, Vol.90 (12), p.2901-2914
Hauptverfasser: Lee, D. Susie, Kang, Yul H. R., Ruiz‐Lambides, Angelina V., Higham, James P.
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creator Lee, D. Susie
Kang, Yul H. R.
Ruiz‐Lambides, Angelina V.
Higham, James P.
description Age‐specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross‐sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long‐lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free‐ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed‐effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age‐dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age‐dependent and age‐independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa. Resumen Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la
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Susie ; Kang, Yul H. R. ; Ruiz‐Lambides, Angelina V. ; Higham, James P.</creator><creatorcontrib>Lee, D. Susie ; Kang, Yul H. R. ; Ruiz‐Lambides, Angelina V. ; Higham, James P.</creatorcontrib><description>Age‐specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross‐sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long‐lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free‐ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed‐effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age‐dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age‐dependent and age‐independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa. Resumen Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la desaparición selectiva. Los datos longitudinales que rastrean la vida reproductiva de individuos específicos son fundamentales, pero tales datos son escasos, especialmente para especies muy longevas como los primates. En este estudio analizamos la trayectoria completa de la fertilidad anual, desde la madurez reproductiva hasta la muerte, de 673 macaco rhesus (Macaca mulatta) hembras que habitan libremente la isla de Cayo Santiago, Puerto Rico. Mostramos que, después de tener en cuenta las diferencias individuales en la fertilidad, el envejecimiento reproductivo exhibe tanto un declive dependiente de la edad, como un declive terminal abrupto independiente de la edad al morir. Aplicando un modelo de cadena de Markov oculta, caracterizamos además el proceso reproductivo subyacente, en el que los individuos pasan por ciclos reproductivos hasta que entran en una condición de fragilidad irreversible que limita la fertilidad. Los resultados proporcionan una valiosa visión de la progresión longitudinal de las trayectorias reproductivas en los primates, al revelar patrones y procesos de senescencia dependientes e independientes de la edad, y contribuyen a un creciente cuerpo de literatura sobre el envejecimiento reproductivo en todos los taxones animales. With a diminishing number of individuals with age, studying the pattern of reproductive ageing has been difficult especially in long‐lived species. The authors characterize the entire reproductive trajectory from 673 free‐ranging female rhesus macaques of Cayo Santiago, and provide clear evidence for both reproductive senescence and age‐independent terminal decline in fertility. Image credit: D. 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Susie</creatorcontrib><creatorcontrib>Kang, Yul H. R.</creatorcontrib><creatorcontrib>Ruiz‐Lambides, Angelina V.</creatorcontrib><creatorcontrib>Higham, James P.</creatorcontrib><title>The observed pattern and hidden process of female reproductive trajectories across the life span in a non‐human primate</title><title>The Journal of animal ecology</title><addtitle>J Anim Ecol</addtitle><description>Age‐specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross‐sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long‐lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free‐ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed‐effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age‐dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age‐dependent and age‐independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa. Resumen Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la desaparición selectiva. Los datos longitudinales que rastrean la vida reproductiva de individuos específicos son fundamentales, pero tales datos son escasos, especialmente para especies muy longevas como los primates. En este estudio analizamos la trayectoria completa de la fertilidad anual, desde la madurez reproductiva hasta la muerte, de 673 macaco rhesus (Macaca mulatta) hembras que habitan libremente la isla de Cayo Santiago, Puerto Rico. Mostramos que, después de tener en cuenta las diferencias individuales en la fertilidad, el envejecimiento reproductivo exhibe tanto un declive dependiente de la edad, como un declive terminal abrupto independiente de la edad al morir. Aplicando un modelo de cadena de Markov oculta, caracterizamos además el proceso reproductivo subyacente, en el que los individuos pasan por ciclos reproductivos hasta que entran en una condición de fragilidad irreversible que limita la fertilidad. Los resultados proporcionan una valiosa visión de la progresión longitudinal de las trayectorias reproductivas en los primates, al revelar patrones y procesos de senescencia dependientes e independientes de la edad, y contribuyen a un creciente cuerpo de literatura sobre el envejecimiento reproductivo en todos los taxones animales. With a diminishing number of individuals with age, studying the pattern of reproductive ageing has been difficult especially in long‐lived species. The authors characterize the entire reproductive trajectory from 673 free‐ranging female rhesus macaques of Cayo Santiago, and provide clear evidence for both reproductive senescence and age‐independent terminal decline in fertility. Image credit: D. 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R.</creatorcontrib><creatorcontrib>Ruiz‐Lambides, Angelina V.</creatorcontrib><creatorcontrib>Higham, James P.</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of animal ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, D. Susie</au><au>Kang, Yul H. R.</au><au>Ruiz‐Lambides, Angelina V.</au><au>Higham, James P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The observed pattern and hidden process of female reproductive trajectories across the life span in a non‐human primate</atitle><jtitle>The Journal of animal ecology</jtitle><addtitle>J Anim Ecol</addtitle><date>2021-12</date><risdate>2021</risdate><volume>90</volume><issue>12</issue><spage>2901</spage><epage>2914</epage><pages>2901-2914</pages><issn>0021-8790</issn><eissn>1365-2656</eissn><abstract>Age‐specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross‐sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long‐lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free‐ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed‐effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age‐dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age‐dependent and age‐independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa. Resumen Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la desaparición selectiva. Los datos longitudinales que rastrean la vida reproductiva de individuos específicos son fundamentales, pero tales datos son escasos, especialmente para especies muy longevas como los primates. En este estudio analizamos la trayectoria completa de la fertilidad anual, desde la madurez reproductiva hasta la muerte, de 673 macaco rhesus (Macaca mulatta) hembras que habitan libremente la isla de Cayo Santiago, Puerto Rico. Mostramos que, después de tener en cuenta las diferencias individuales en la fertilidad, el envejecimiento reproductivo exhibe tanto un declive dependiente de la edad, como un declive terminal abrupto independiente de la edad al morir. Aplicando un modelo de cadena de Markov oculta, caracterizamos además el proceso reproductivo subyacente, en el que los individuos pasan por ciclos reproductivos hasta que entran en una condición de fragilidad irreversible que limita la fertilidad. Los resultados proporcionan una valiosa visión de la progresión longitudinal de las trayectorias reproductivas en los primates, al revelar patrones y procesos de senescencia dependientes e independientes de la edad, y contribuyen a un creciente cuerpo de literatura sobre el envejecimiento reproductivo en todos los taxones animales. With a diminishing number of individuals with age, studying the pattern of reproductive ageing has been difficult especially in long‐lived species. 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subjects Age
Aging
Animals
Cross-Sectional Studies
Death
Ecology
Evolution
Female
Fertility
hidden Markov chain model
Life span
Longevity
Macaca mulatta
Markov chains
Mathematical models
Mortality
Population structure
Primates
Reproduction
reproductive ageing
Senescence
terminal decline
title The observed pattern and hidden process of female reproductive trajectories across the life span in a non‐human primate
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