The long reach of family ties

doi:10.1126/science.abj5234

GSTDTAP > 气候变化

DOI	10.1126/science.abj5234
	The long reach of family ties
	Josh A. Firth; Ben C. Sheldon
	2021-07-16
发表期刊	Science
出版年	2021
英文摘要	The social structure of a population shapes many aspects of individuals' lives. Network analysis details how individuals are tied to one another within a “social network” ([ 1 ][1]). Although the relevance of social networks for behavior and ecology is becoming well established, the processes that govern their underlying structure, and individuals' social positions relative to others, are less well known ([ 2 ][2]). On p. 348 of this issue, Ilany et al. ([ 3 ][3]) apply social network analysis to a population of wild spotted hyenas over 27 years and spanning multiple hyena generations. Their findings support a proposed model ([ 2 ][2]) that inheritance of social network ties—specifically that offsprings' social bonds are derived from their mothers' social affiliates—plays a key role in shaping social structure across generations. Furthermore, these inherited networks may be linked to survival, providing a potential selective force that promotes the evolution of the inheritance of social networks. Generally, the emergent properties of animal societies can be thought of as resulting from individual-level variation in behavior and individuals' interactions with others ([ 1 ][1]). Because these behaviors might have quite simple bases, but nevertheless lead to complex social network structures ([ 4 ][4]), it is reasonable to suggest that social network properties of individuals might have heritable components. Evidence from a range of organisms, from humans to fruit flies ([ 5 ][5]), supports this. However, what Ilany et al. demonstrate is an altogether richer phenomenon. Through combining detailed observations with social network analysis, they demonstrate that the specific social relationships of hyenas resemble those of their mothers; that this resemblance persists for many years, even after parent-offspring social relationships weaken; that offspring of higher-ranking mothers and with closer bonds to their mothers inherit their social networks to a greater degree; and that this greater degree of social network inheritance even predicts increased survival of the offspring and of the mother. Hence, rather than the social tendencies of offspring resembling that of their parents, it is the specific social networks that are inherited (see the figure). Ilany et al. provide new insights into the generation of variation in social structure and into how inheritance and sociality interact, but their results also have wider implications. The consequences of network structure have been well demonstrated for the interacting individuals within generations ([ 1 ][1]). However, if specific interactions carry over into subsequent generations, this transgenerational legacy in social interactions between similar genotypes (albeit different individuals) from year to year has implications for understanding processes that coevolve with social behavior. Social inheritance of association networks causes a strong covariance between the many consequences of social structure and inherited genetic variation over generations. The consequences of such social inheritance for social transmission and the evolution of social interactions are particularly interesting. A prominent example of social transmission relates to the spread of pathogens and other microbiota ([ 1 ][1], [ 6 ][6]). When social structure persists across generations through inheritance, and susceptibility or immunity is also inherited, it creates a link between these and could either increase vulnerability to disease (through disease persisting in susceptible groups across generations) or decrease risk (through immunity or reduced susceptibility within clusters). For example, imagine a pathogen whose transmission probability is determined by specific gene-for-gene matching with hosts; under this model of social inheritance, parents and offspring are much more likely to be exposed to the same specific lineages of microbes and vice versa, and coevolutionary interactions between host and pathogen genomes may be accelerated. Helpful bacteria are also spread socially for many species, particularly skin and gut microbiota ([ 7 ][7]), for which transmission occurs both vertically (from parent to offspring) and horizontally (between peers). As such, inheritance of social interactions across generations, in which individuals inherit social associations from a parent, should contribute to stabilizing the composition of these communities through promoting persistence of particular socially spread microbiota and reducing mixing across generations. In almost all social systems, diverse types of information are also socially transmitted between individuals. Information can spread across social networks as individuals gain new information, adopt the behavior, and then transmit this to others ([ 6 ][6], [ 8 ][8]). Unlike infectious diseases, however, these “behavioral contagions” frequently depend on much more than exposure to contagious individuals. Individual decisions surrounding whether to adopt a socially informed behavior may, for example, depend on whether they conform with the majority of the population, or which of their specific associates are performing the behavior, even in relatively simple animal systems ([ 9 ][9]). These “social learning strategies” ([ 10 ][10]) can cause behaviors to spread more efficiently on heavily clustered social networks rather than diffusely connected networks that often facilitate disease transmission ([ 8 ][8]). Therefore, just as the inheritance of social ties that Ilany et al. demonstrate forces social networks into clustered structures that persist across generations, this may also promote the spread and establishment of socially informed behaviors within groups compared with systems without social inheritance. Furthermore, social inheritance and the resulting cross-generational clustered networks of this kind may support the development of behavioral traditions or animal “cultures,” which require the initial social spread of behaviors and the maintenance of these particular behaviors over time as individuals learn these from their group members ([ 11 ][11]) both between and within generations. ![Figure][12] A network view of social inheritanceGRAPHIC: N. CARY/ SCIENCE There is a rich theoretical literature that stresses the relevance of social network structure for the evolution of cooperation ([ 12 ][13]). The type of social inheritance demonstrated by Ilany et al. implies that interactions between specific genotypes persist across generations and hence greatly increase the persistence of such interactions as well as the chance for reciprocation of cooperative actions. The transgenerational carryover of social structure also implies that competition will be occurring between the same interacting genotypes more than by chance, and that this presents the opportunity for reduced competition through prior familiarity—sometimes called the “dear enemy effect”—to occur across generations. Although the study of Ilany et al. , and prior modeling ([ 2 ][2]), has focused on social inheritance through kin-structuring, another open question is whether the same process could operate in non–kin-structured systems, too. For example, any animal (or plant) population for which offspring show limited dispersal might result in an increased tendency for offspring to interact socially with the same individuals whom their parents interacted with, or even with the offspring of those individuals whom their parents interacted with. As such, the existence of social inheritance provides a general potential for the social choices of the parents to directly influence the social setting of their offspring. Future work should seek to examine how widely specific social relationships are inherited in range of population structures and what implications this has for the rate of evolution of the many processes that depend on social network structure. 1. [↵][14]1. J. Krause, 2. R. James, 3. D. W. Franks, 4. D. P. Croft , Animal Social Networks (Oxford Univ. Press, 2015). 2. [↵][15]1. A. Ilany, 2. E. Akçay , Nat. Commun. b, 12084 (2016). [OpenUrl][16] 3. [↵][17]1. A. Ilany, 2. K. E. Holekamp, 3. E. Akçay , Science 373, 348 (2021). [OpenUrl][18][Abstract/FREE Full Text][19] 4. [↵][20]1. J. A. Firth, 2. B. C. Sheldon, 3. L. J. N. Brent , P. Roy. Soc. B Biol. Sci. 284, 20171939 (2017). [OpenUrl][21] 5. [↵][22]1. E. W. Wice, 2. J. B. Saltz , Nat. Commun. 12, 3357 (2021). [OpenUrl][23] 6. [↵][24]1. A. Kucharski , Rules of Contagion: Why Things Spread—And Why They Stop (Profile Books, 2020). 7. [↵][25]1. A. Sarkar et al ., Nat. Ecol. Evol. 4, 1020 (2020). [OpenUrl][26] 8. [↵][27]1. D. Centola , How Behaviour Spreads: The Science of Complex Contagions (Princeton Univ. Press, 2018). 9. [↵][28]1. J. A. Firth , Trends Ecol. Evol. 35, 100 (2020). [OpenUrl][29] 10. [↵][30]1. W. Hoppitt, 2. K. N. Laland , Social Learning An Introduction to Mechanisms, Methods, and Models. (Princeton Univ. Press, 2013). 11. [↵][31]1. L. M. Aplin et al ., Nature 518, 538 (2015). [OpenUrl][32][CrossRef][33][PubMed][34] 12. [↵][35]1. S. Gokcekus, 2. E. F. Cole, 3. B. C. Sheldon, 4. J. A. Firth , Biol. Rev. Camb. Philos. Soc. (2021). 10.111/brv.12757 Acknowledgments: This work was supported by the Biotechnology and Biological Sciences Research Council (BB/S009752/1) and Natural Environment Research Council (NE/S010335/1). 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领域	气候变化 ; 资源环境
URL	查看原文
引用统计
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/334343
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Josh A. Firth,Ben C. Sheldon. The long reach of family ties[J]. Science,2021.
APA	Josh A. Firth,&Ben C. Sheldon.(2021).The long reach of family ties.Science.
MLA	Josh A. Firth,et al."The long reach of family ties".Science (2021).