Juvenile rank acquisition is associated with fitness independent of adult rank

Abstract

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.

Early‐life relationships matter: Social position during early life predicts fitness among female spotted hyenas

“…consistently predict either its ARS or its longevity. Although it has been well-documented that maternal rank affects juvenile survivorship in this species (Strauss, Shizuka, & Holekamp, 2020;Watts et al, 2009), of those hyenas who survived past 3 years of age in our study, their ranks early in life did not always predict their fitness in adulthood. However, regardless of the rank an individual held early in life, its early social position within its network strongly influenced its ARS and longevity.…”

Social groups buffer maternal loss in mountain gorillas

“…In these species, one of the major mechanisms posited to link maternal loss with increased mortality is through the social adversity caused by mother absence. Specifically, mother absence is found to reduce social integration 5,21 , competitivity 16,22 , dominance rank 6,18–20 and opportunities for social learning 8,23,24,26 . But the lack of increased mortality in gorillas and certain human populations suggests that mother absence does not always lead to social adversity in mammals with extended maternal care.…”

“…In social mammals the removal of maternal care due to maternal loss can reduce survival in the youngest offspring 3 by affecting for example nutrition, thermoregulation and protection 4 . But maternal loss can also reduce the fitness of offspring in a far broader age range through long-term effects on their social environment, negatively influencing their social integration and social status throughout their lives 1,5,6 . Multiple studies have now confirmed effects on survivorship for individuals orphaned well past the period of nutritional dependency, with these negative changes to their social environment, often termed social adversity, posited to be the key mechanism by which this occurs 5,7–10 .…”

“…Several studies have demonstrated the specific social benefits that mothers provide to co-residing offspring, which can extend well into adulthood 7,8,16,17 . In some societies the active support of mothers can increase the rank of their offspring 6,18–20 with higher ranking individuals showing greater survival in almost all natural animal populations in which it has been studied 1 . In baboons, where female rank is inherited from the mother, mothers play a key role in integrating their offspring within the larger social group 5 .…”

Early maternal loss affects diurnal cortisol slopes in immature but not mature wild chimpanzees

“…In mammals, mothers are essential for the early development of their infants since they provide post-natal care (Maestripieri & Mateo 2009). Maternal loss in mammals reduces growth (Samuni et al 2020), survival (Watts et al 2009;Andres et al 2013;Tung et al 2016;Stanton et al 2020), and long-term reproductive success (Andres et al 2013;Strauss et al 2020;Crockford et al 2020, reviewed in Clutton-Brock 2016. The biological embedding model (Power & Hertzman 1997;Miller et al 2011;Berens et al 2017) posits that adversity experienced early in life, including exposure to severe stressors, can have deleterious consequences on an individual's physiology and health across their lifespan.…”