How social development in early-life affects fitness remains poorly understood.
2. Though there is growing evidence that early-life relationships can affect fitness,
little research has investigated how social positions develop or whether there are
particularly important periods for social position development in an animal's life
history. In long-lived species in particular, understanding the lasting consequences
of early-life social environments requires detailed, long-term datasets.
3. Here we used a 25-year dataset to test whether social positions held during early
development predicted adult fitness. Specifically, we quantified social position
using three social network metrics: degree, strength and betweenness. We determined
the social position of each individual in three types of networks during
each of three stages of ontogeny to test whether they predict annual reproductive
success (ARS) or longevity among adult female spotted hyenas Crocuta crocuta.
4. The social positions occupied by juvenile hyenas did predict their fitness, but the
effects of social position on fitness measures differed between stages of early development.
Network metrics when individuals were young adults better predicted
ARS, but network metrics for younger animals, particularly when youngsters were
confined to the communal den, better predicted longevity than did metrics assessed
during other stages of development.
5. Our study shows how multiple types of social bonds formed during multiple stages
of social development predict lifetime fitness outcomes. We suggest that social
bonds formed during specific phases of development may be more important than
others when considering fitness outcomes.
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Juvenile rank acquisition is associated with fitness independent of adult rank
Social rank is a significant determinant of fitness in a variety of species. The importance of social rank suggests that the process by which juveniles come to establish their position in the social hierarchy is a critical component of development. Here, we use the highly predictable process of rank acquisition in spotted hyenas to study the consequences of variation in rank acquisition in early life. In spotted hyenas, rank is ‘inherited’ through a learning process called ‘maternal rank inheritance.’ This pattern is very consistent: approximately 80% of juveniles acquire the exact rank expected under the rules of maternal rank inheritance. The predictable nature of rank acquisition in these societies allows the process of rank acquisition to be studied independently from the ultimate rank that each juvenile attains. In this study, we use Elo-deviance scores, a novel application of the Elo-rating method, to calculate each juvenile's deviation from the expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition among juveniles, most of these juveniles come to attain the exact rank expected of them according to the rules of maternal rank inheritance. Nevertheless, we find that transient variation in rank acquisition in early life is associated with long-term fitness consequences for these individuals: juveniles ‘underperforming’ their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers, and this relationship is independent of both maternal rank and rank achieved in adulthood. We also find that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness. Future work is needed to determine if variation in rank acquisition directly affects fitness, or if some other variable, such as maternal investment or juvenile condition, causes variation in both of these outcomes.
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- Award ID(s):
- 1755089
- NSF-PAR ID:
- 10149799
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 287
- Issue:
- 1922
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20192969
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract How social development in early‐life affects fitness remains poorly understood.
Though there is growing evidence that early‐life relationships can affect fitness, little research has investigated how social positions develop or whether there are particularly important periods for social position development in an animal's life history. In long‐lived species in particular, understanding the lasting consequences of early‐life social environments requires detailed, long‐term datasets.
Here we used a 25‐year dataset to test whether social positions held during early development predicted adult fitness. Specifically, we quantified social position using three social network metrics: degree, strength and betweenness. We determined the social position of each individual in three types of networks during each of three stages of ontogeny to test whether they predict annual reproductive success (ARS) or longevity among adult female spotted hyenas
Crocuta crocuta .The social positions occupied by juvenile hyenas did predict their fitness, but the effects of social position on fitness measures differed between stages of early development. Network metrics when individuals were young adults better predicted ARS, but network metrics for younger animals, particularly when youngsters were confined to the communal den, better predicted longevity than did metrics assessed during other stages of development.
Our study shows how multiple types of social bonds formed during multiple stages of social development predict lifetime fitness outcomes. We suggest that social bonds formed during specific phases of development may be more important than others when considering fitness outcomes.
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Social hierarchies are widespread in human and animal societies, and an individual’s position in its hierarchy affects both its access to resources and its fitness. Hierarchies are traditionally thought of in terms of variation in individual ability to win fights, but many are structured around arbitrary conventions like nepotistic inheritance rather than such traits as physical strength or weapon size. These convention-based societies are perplexing because position in the hierarchy appears to be gained irrespective of individual physical ability, yet social status strongly affects access to resources and fitness. It remains unclear why individuals abide by seemingly arbitrary conventions regarding social status when they stand to benefit by ignoring these conventions and competing for top positions or access to resources. Using data from wild spotted hyenas collected over 27 y and five generations, we show that individuals who repeatedly form coalitions with their top allies are likely to improve their position in the hierarchy, suggesting that social alliances facilitate revolutionary social change. Using lifetime reproductive success as a fitness measure, we go on to demonstrate that these status changes can have major fitness consequences. Finally, we show that the consequences of these changes may become even more dramatic over multiple generations, as small differences in social rank become amplified over time. This work represents a first step in reconciling the advantages of high status with the appearance of “arbitrary” conventions that structure inequality in animal and human societies.
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The structure of animal social networks influences survival and reproductive success, as well as pathogen and information transmission. However, the general mechanisms determining social structure remain unclear. Using data from 73,767 social interactions among wild spotted hyenas collected over 27 years, we show that the process of social inheritance determines how offspring relationships are formed and maintained. Relationships between offspring and other hyenas bear resemblance to those of their mothers for as long as 6 years, and the degree of similarity increases with maternal social rank. Mother-offspring relationship strength affects social inheritance and is positively correlated with offspring longevity. These results support the hypothesis that social inheritance of relationships can structure animal social networks and be subject to adaptive tradeoffs.
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Abstract Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross‐sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (
Crocuta crocuta ) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high‐ than low‐ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2019.2969
