Josh A Firth, Gregory F Albery, Sandra Bouwhuis, Lauren J N Brent, Roberto Salguero-Gómez
{"title":"Understanding age and society using natural populations.","authors":"Josh A Firth, Gregory F Albery, Sandra Bouwhuis, Lauren J N Brent, Roberto Salguero-Gómez","doi":"10.1098/rstb.2022.0469","DOIUrl":"10.1098/rstb.2022.0469","url":null,"abstract":"<p><p>Ageing affects almost all aspects of life and therefore is an important process across societies, human and non-human animal alike. This article introduces new research exploring the complex interplay between individual-level ageing and demography, and the consequences this interplay holds for the structure and functioning of societies across various natural populations. We discuss how this Special Issue provides a foundation for integrating perspectives from evolutionary biology, behavioural ecology and demography to provide new insights into how ageing shapes individuals' social behaviour and social associations, and how this in turn impacts social networks, social processes (such as disease or information transfer) and fitness. Through examining these topics across taxa, from invertebrates to birds and mammals, we outline how contemporary studies are using natural populations to advance our understanding of the relationship between age and society in innovative ways. We highlight key emerging research themes from this Special Issue, such as how sociality affects lifespan and health, the genetic and ecological underpinnings of social ageing and the adaptive strategies employed by different species. We conclude that this Special Issue underscores the importance of studying social ageing using diverse systems and interdisciplinary approaches for advancing evolutionary and ecological insights into both ageing and sociality more generally.This article is part of the discussion meeting issue 'Understanding age and society using natural populations '.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220469"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513640/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505473","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Social ageing and higher-order interactions: social selectiveness can enhance older individuals' capacity to transmit knowledge.","authors":"Matthew J Hasenjager, Nina H Fefferman","doi":"10.1098/rstb.2022.0461","DOIUrl":"10.1098/rstb.2022.0461","url":null,"abstract":"<p><p>In long-lived organisms, experience can accumulate with age, such that older individuals may act as repositories of ecological and social knowledge. Such knowledge is often beneficial and can spread via social transmission, leading to the expectation that ageing individuals will remain socially well-integrated. However, social ageing involves multiple processes that modulate the relationship between age and social connectivity in complex ways. We developed a generative model to explore how social ageing may drive changes in social network position and shape older individuals' capacity to transmit knowledge to others. We further employ novel hypernetwork analyses that capture higher-order interactions (i.e. involving ≥ 3 participants) to reveal potential relationships between age and sociality that conventional dyadic networks may overlook. We find that older individuals in our simulations effectively facilitate transmission across a range of scenarios, especially when transmission resembles a complex contagion or when social selectivity (i.e. prioritization of key relationships) rapidly emerges with age. These patterns result from the formation of tight-knit sets of older associates that co-occur in multiple groups, thereby reinforcing one another's capacity to transmit knowledge. Our findings suggest key avenues for future empirical work and illustrate the use of hypernetworks in advancing the study of social behaviour.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220461"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513644/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505568","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Erin R Siracusa, Melissa A Pavez-Fox, Josué E Negron-Del Valle, Daniel Phillips, Michael L Platt, Noah Snyder-Mackler, James P Higham, Lauren J N Brent, Matthew J Silk
{"title":"Social ageing can protect against infectious disease in a group-living primate.","authors":"Erin R Siracusa, Melissa A Pavez-Fox, Josué E Negron-Del Valle, Daniel Phillips, Michael L Platt, Noah Snyder-Mackler, James P Higham, Lauren J N Brent, Matthew J Silk","doi":"10.1098/rstb.2022.0462","DOIUrl":"10.1098/rstb.2022.0462","url":null,"abstract":"<p><p>The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals' lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of 'social ageing' depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence the evolutionary dynamics of social ageing in natural populations.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220462"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11528358/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505469","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gregory F Albery, Adam Z Hasik, Sean Morris, Alison Morris, Fiona Kenyon, David McBean, Josephine M Pemberton, Daniel H Nussey, Josh A Firth
{"title":"Divergent age-related changes in parasite infection occur independently of behaviour and demography in a wild ungulate.","authors":"Gregory F Albery, Adam Z Hasik, Sean Morris, Alison Morris, Fiona Kenyon, David McBean, Josephine M Pemberton, Daniel H Nussey, Josh A Firth","doi":"10.1098/rstb.2023.0508","DOIUrl":"10.1098/rstb.2023.0508","url":null,"abstract":"<p><p>As animals age, they exhibit a suite of phenotypic changes, often including reductions in movement and social behaviour ('behavioural ageing'). By altering an individual's exposure to parasites, behavioural ageing may influence infection status trajectories over the lifespan. However, these processes could be confounded by age-related changes in other phenotypic traits, or by selective disappearance of certain individuals owing to parasite-induced mortality. Here, we uncover contrasting age-related patterns of infection across three helminth parasites in wild adult female red deer (<i>Cervus elaphus</i>). Counts of strongyle nematodes (order: Strongylida) increased with age, while counts of liver fluke (<i>Fasciola hepatica</i>) and tissue worm (<i>Elaphostrongylus cervi</i>) decreased, and lungworm (<i>Dictyocaulus</i>) counts did not change. These relationships could not be explained by socio-spatial behaviours, spatial structuring, or selective disappearance, suggesting behavioural ageing is unlikely to be responsible for driving age trends. Instead, social connectedness and strongyle infection were positively correlated, such that direct age-infection trends were directly contrasted with the effects implied by previously documented behavioural ageing. This suggests that behavioural ageing may reduce parasite exposure, potentially countering other age-related changes. These findings demonstrate that different parasites can show contrasting age trajectories depending on diverse intrinsic and extrinsic factors, and that behaviour's role in these processes is likely to be complex and multidirectional.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20230508"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513643/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505562","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Agents seeking long-term access to the wisdom of the crowd reduce immediate decision-making accuracy.","authors":"Richard P Mann","doi":"10.1098/rstb.2022.0467","DOIUrl":"10.1098/rstb.2022.0467","url":null,"abstract":"<p><p>Living in groups offers social animals the significant advantage of accessing collective wisdom and enhanced information processing, enabling more accurate decisions related to foraging, navigation and habitat selection. Preserving group membership is crucial for sustaining access to collective wisdom, incentivizing animals to prioritize group cohesion. However, when individuals encounter divergent information about the quality of various options, this can create a conflict between pursuing immediate rewards and the maintenance of group membership to improve access to future pay-offs. In this study, I show that rational agents who seek to maximize long-term rewards will be more inclined to follow the decisions of their peers than those with short-term horizons. In doing so, they necessarily make less-rewarding decisions in the short-term, which manifests in a lower individual accuracy when choosing the better of two options. Furthermore, I demonstrate that intuitions about collective wisdom can be misleading in groups of agents who prioritize long-term rewards, with disagreement being a better signal for the accuracy of collective choices than consensus. These results demonstrate that observed patterns of sociality should be interpreted in the context of the life history of an individual and its peers, rather than through the lens of an isolated decision.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220467"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11528357/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505561","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Julia Schroeder, Jamie Dunning, Alex Hoi Han Chan, Heung Ying Janet Chik, Terry Burke
{"title":"Not so social in old age: demography as one driver of decreasing sociality.","authors":"Julia Schroeder, Jamie Dunning, Alex Hoi Han Chan, Heung Ying Janet Chik, Terry Burke","doi":"10.1098/rstb.2022.0458","DOIUrl":"10.1098/rstb.2022.0458","url":null,"abstract":"<p><p>Humans become more selective with whom they spend their time, and as a result, the social networks of older humans are smaller than those of younger ones. In non-human animals, processes such as competition and opportunity can result in patterns of declining sociality with age. While there is support for declining sociality with age in mammals, evidence from wild bird populations is lacking. Here, we test whether sociality declines with age in a wild, insular bird population, where we know the exact ages of individuals. Using 6 years of sociality data, we find that as birds aged, their degree and betweenness decreased. The number of same-age birds still alive also decreased with age. Our results suggest that a longitudinal change in sociality with age may be, in part, an emergent effect of natural changes in demography. This highlights the need to investigate the changing costs and benefits of sociality across a lifetime.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220458"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513642/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505566","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Fernando A Campos, Eva C Wikberg, Joseph D Orkin, Yeonjoo Park, Noah Snyder-Mackler, Saul Cheves Hernandez, Ronald Lopez Navarro, Linda M Fedigan, Michael Gurven, James P Higham, Katharine M Jack, Amanda D Melin
{"title":"Wild capuchin monkeys as a model system for investigating the social and ecological determinants of ageing.","authors":"Fernando A Campos, Eva C Wikberg, Joseph D Orkin, Yeonjoo Park, Noah Snyder-Mackler, Saul Cheves Hernandez, Ronald Lopez Navarro, Linda M Fedigan, Michael Gurven, James P Higham, Katharine M Jack, Amanda D Melin","doi":"10.1098/rstb.2023.0482","DOIUrl":"10.1098/rstb.2023.0482","url":null,"abstract":"<p><p>Studying biological ageing in animal models can circumvent some of the confounds exhibited by studies of human ageing. Ageing research in non-human primates has provided invaluable insights into human lifespan and healthspan. Yet data on patterns of ageing from wild primates remain relatively scarce, centred around a few populations of catarrhine species. Here, we introduce the white-faced capuchin, a long-lived platyrrhine primate, as a promising new model system for ageing research. Like humans, capuchins are highly social, omnivorous generalists, whose healthspan and lifespan relative to body size exceed that of other non-human primate model species. We review recent insights from capuchin ageing biology and outline our expanding, integrative research programme that combines metrics of the social and physical environments with physical, physiological and molecular hallmarks of ageing across the natural life courses of multiple longitudinally tracked individuals. By increasing the taxonomic breadth of well-studied primate ageing models, we generate new insights, increase the comparative value of existing datasets to geroscience and work towards the collective goal of developing accurate, non-invasive and reliable biomarkers with high potential for standardization across field sites and species, enhancing the translatability of primate studies.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20230482"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513648/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505474","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Age-dependent shaping of the social environment in a long-lived seabird: a quantitative genetic approach.","authors":"Maria Moiron, Sandra Bouwhuis","doi":"10.1098/rstb.2022.0465","DOIUrl":"10.1098/rstb.2022.0465","url":null,"abstract":"<p><p>Individual differences in social behaviour can result in fine-scale variation in spatial distribution and, hence, in the social environment experienced. Given the expected fitness consequences associated with differences in social environments, it is imperative to understand the factors that shape them. One potential such factor is age. Age-specific social behaviour-often referred to as 'social ageing'-has only recently attracted attention, requiring more empirical work across taxa. Here, we use 29 years of longitudinal data collected in a pedigreed population of long-lived, colonially breeding common terns (<i>Sterna hirundo</i>) to investigate sources of variation in, and quantitative genetic underpinnings of, an aspect of social ageing: the shaping of the social environment experienced, using the number of neighbours during breeding as a proxy. Our analyses reveal age-specific declines in the number of neighbours during breeding, as well as selective disappearance of individuals with a high number of neighbours. Moreover, we find this social trait, as well as individual variation in the slope of its age-specific decline, to be heritable. These results suggest that social ageing might underpin part of the variation in the overall multicausal ageing phenotype, as well as undergo microevolution, highlighting the potential role of social ageing as a facilitator for, or constraint of, the evolutionary potential of natural populations.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20220465"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513638/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Phoebe A Cook, Robin A Costello, Edmund D Brodie Iii, Vincent Formica
{"title":"Population age structure shapes selection on social behaviour in a long-lived insect.","authors":"Phoebe A Cook, Robin A Costello, Edmund D Brodie Iii, Vincent Formica","doi":"10.1098/rstb.2023.0331","DOIUrl":"10.1098/rstb.2023.0331","url":null,"abstract":"<p><p>Social traits are expected to experience highly context-dependent selection, but we know little about the contextual factors that shape selection on social behaviours. We hypothesized that the fitness consequences of social interactions will depend on the age of social partners, and therefore that population age structure will shape evolutionary pressures on sociality. Here, we investigate the consequences of age variation at multiple levels of social organization for both individual fitness and sexual selection on social network traits. We experimentally manipulated the age composition of populations of the forked fungus beetle <i>Bolitotherus cornutus</i>, creating 12 replicate populations with either young or old age structures. We found that fitness is associated with variance in age at three different levels of organization: the individual, interacting social partners, and the population. Older individuals have higher reproductive success, males pay a fitness cost when they interact with old males and females achieve lower fitness in older populations. In addition to influencing fitness, population age structure also altered the selection acting on social network position in females. Female sociality is under positive selection only in old populations. Our results highlight age structure as an understudied demographic variable shaping the landscape of selection on social behaviour.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.</p>","PeriodicalId":5,"journal":{"name":"ACS Applied Materials & Interfaces","volume":"379 1916","pages":"20230331"},"PeriodicalIF":5.4,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11513641/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142505567","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ravi Chidambaram, Kamal Kumar, Smriti Parashar, Gowsalya Ramachandran, Shuliang Chen, Susan Ferro-Novick
{"title":"PINK1 controls RTN3L-mediated ER autophagy by regulating peripheral tubule junctions.","authors":"Ravi Chidambaram, Kamal Kumar, Smriti Parashar, Gowsalya Ramachandran, Shuliang Chen, Susan Ferro-Novick","doi":"10.1083/jcb.202407193","DOIUrl":"https://doi.org/10.1083/jcb.202407193","url":null,"abstract":"<p><p>Here, we report that the RTN3L-SEC24C endoplasmic reticulum autophagy (ER-phagy) receptor complex, the CUL3KLHL12 E3 ligase that ubiquitinates RTN3L, and the FIP200 autophagy initiating protein, target mutant proinsulin (Akita) condensates for lysosomal delivery at ER tubule junctions. When delivery was blocked, Akita condensates accumulated in the ER. In exploring the role of tubulation in these events, we unexpectedly found that loss of the Parkinson's disease protein, PINK1, reduced peripheral tubule junctions and blocked ER-phagy. Overexpression of the PINK1 kinase substrate, DRP1, increased junctions, reduced Akita condensate accumulation, and restored lysosomal delivery in PINK1-depleted cells. DRP1 is a dual-functioning protein that promotes ER tubulation and severs mitochondria at ER-mitochondria contact sites. DRP1-dependent ER tubulating activity was sufficient for suppression. Supporting these findings, we observed PINK1 associating with ER tubules. Our findings show that PINK1 shapes the ER to target misfolded proinsulin for RTN3L-SEC24C-mediated macro-ER-phagy at defined ER sites called peripheral junctions. These observations may have important implications for understanding Parkinson's disease.</p>","PeriodicalId":15211,"journal":{"name":"Journal of Cell Biology","volume":"223 12","pages":""},"PeriodicalIF":7.4,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142648187","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}