scholarly journals Juvenile rank acquisition influences fitness independent of adult rank

2019 ◽  
Author(s):  
Eli D Strauss ◽  
Daizaburo Shizuka ◽  
Kay E Holekamp

AbstractSocial rank has been identified as 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 social 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 highly predictable: ~80% of juveniles acquire the exact rank predicted by the rules of maternal rank inheritance. This 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 a novel application of the Elo-rating method to calculate each juvenile’s deviation from expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition in 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 predicts long term fitness consequences for these individuals: juveniles ‘underperforming’ their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers. Finally, we present evidence that this variability in rank acquisition in early life represents a source of early life adversity, and that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness.

2020 ◽  
Vol 287 (1922) ◽  
pp. 20192969 ◽  
Author(s):  
Eli D. Strauss ◽  
Daizaburo Shizuka ◽  
Kay E. Holekamp

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.


2020 ◽  
Vol 117 (40) ◽  
pp. 24909-24919 ◽  
Author(s):  
Chelsea J. Weibel ◽  
Jenny Tung ◽  
Susan C. Alberts ◽  
Elizabeth A. Archie

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.


2015 ◽  
Vol 282 (1813) ◽  
pp. 20151167 ◽  
Author(s):  
Vérane Berger ◽  
Jean-François Lemaître ◽  
Dominique Allainé ◽  
Jean-Michel Gaillard ◽  
Aurélie Cohas

Evidence that the social environment at critical stages of life-history shapes individual trajectories is accumulating. Previous studies have identified either current or delayed effects of social environments on fitness components, but no study has yet analysed fitness consequences of social environments at different life stages simultaneously. To fill the gap, we use an extensive dataset collected during a 24-year intensive monitoring of a population of Alpine marmots ( Marmota marmota ), a long-lived social rodent. We test whether the number of helpers in early life and over the dominance tenure length has an impact on litter size at weaning, juvenile survival, longevity and lifetime reproductive success (LRS) of dominant females. Dominant females, who were born into a group containing many helpers and experiencing a high number of accumulated helpers over dominance tenure length showed an increased LRS through an increased longevity. We provide evidence that in a wild vertebrate, both early and adult social environments influence individual fitness, acting additionally and independently. These findings demonstrate that helpers have both short- and long-term effects on dominant female Alpine marmots and that the social environment at the time of birth can play a key role in shaping individual fitness in social vertebrates.


2007 ◽  
Vol 90 (1) ◽  
pp. 85-95 ◽  
Author(s):  
KRISTIN A. SCHUBERT ◽  
DANIEL J. MENNILL ◽  
SCOTT M. RAMSAY ◽  
KEN A. OTTER ◽  
PETER T. BOAG ◽  
...  

Animals ◽  
2019 ◽  
Vol 9 (6) ◽  
pp. 316 ◽  
Author(s):  
Jocelyn M. Woods ◽  
Stephen R. Ross ◽  
Katherine A. Cronin

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social factors, such as social rank, can also have a large impact on behavior. Here, we considered the influence of both the role of visitors (crowd size and activity levels) and rank on the occurrence of visitor-directed aggression by zoo-housed Japanese macaques (Macaca fuscata, N = 12). We conducted 52 weeks of observation (443.8 h) of macaques living in a large outdoor habitat and recorded 1574 events of visitor-directed behavior, 94.2% of which was characterized as aggressive. We calculated rank using the Elo-rating method. GLMM comparisons indicate that rank was a significant predictor of visitor-directed aggression, with lower-ranked individuals displaying more frequent aggression towards visitors. Additionally, visitor-directed aggression differed by crowd activity levels, but not crowd size. These results support our prediction that rank is associated with differences in visitor-directed aggression, and we interpret this pattern as lower-ranking macaques redirecting aggression toward zoo visitors as safe targets. This work emphasizes how factors emanating from the zoo environment can combine with social dynamics to influence primate response to human presence in the zoo setting.


2017 ◽  
Vol 284 (1861) ◽  
pp. 20171383 ◽  
Author(s):  
Dominic L. Cram ◽  
Pat Monaghan ◽  
Robert Gillespie ◽  
Tim Clutton-Brock

Early-life adversity can affect health, survival and fitness later in life, and recent evidence suggests that telomere attrition may link early conditions with their delayed consequences. Here, we investigate the link between early-life competition and telomere length in wild meerkats. Our results show that, when multiple females breed concurrently, increases in the number of pups in the group are associated with shorter telomeres in pups. Given that pups from different litters compete for access to milk, we tested whether this effect is due to nutritional constraints on maternal milk production, by experimentally supplementing females' diets during gestation and lactation. While control pups facing high competition had shorter telomeres, the negative effects of pup number on telomere lengths were absent when maternal nutrition was experimentally improved. Shortened pup telomeres were associated with reduced survival to adulthood, suggesting that early-life competition for nutrition has detrimental fitness consequences that are reflected in telomere lengths. Dominant females commonly kill pups born to subordinates, thereby reducing competition and increasing growth rates of their own pups. Our work suggests that an additional benefit of infanticide may be that it also reduces telomere shortening caused by competition for resources, with associated benefits for offspring ageing profiles and longevity.


2020 ◽  
Author(s):  
Sam K Patterson ◽  
Katie Hinde ◽  
Angela B Bond ◽  
Benjamin C Trumble ◽  
Shirley C Strum ◽  
...  

Adverse experiences during early life exert important effects on development, health, reproduction, and social bonds, with consequences often persisting across generations. A mother's early life experiences can impact her offspring's development through a number of pathways, such as maternal care, physiological signaling through glucocorticoids, or even intergenerational effects like epigenetic inheritance. Early life adversity in female yellow baboons (Papio cynocephalus) predicts elevated glucocorticoids, reduced sociality, shortened lifespan, and higher offspring mortality. If baboon mothers with more early life adversity, experience poorer condition and struggle to provide for their offspring, this could contribute to the persisting transgenerational effects of adversity. Here, we examined the effects of mothers' early life adversity on their maternal effort, physiology, and offspring survivability in a population of olive baboons, Papio anubis. Mothers who experienced more adversity in their own early development exerted greater maternal effort (i.e., spent more time nursing and carrying) and had higher glucocorticoid metabolites than mothers with less early life adversity. Offspring of mothers with more early life adversity had reduced survivability compared to offspring of mothers with less early life adversity. There was no evidence that high maternal social rank buffered against the effects of early life adversity. Our data suggest early life experiences can have lasting consequences on maternal effort and physiology, which may function as proximate mechanisms for intergenerational effects of maternal experience.


2020 ◽  
Author(s):  
Yannick Auclair ◽  
Nina Gerber ◽  
Barbara König ◽  
Anna K. Lindholm

AbstractIn mammals, reproduction is influenced by competitive stress, temperature and food availability and these factors might be crucial already during early life. Favourable early life environment and high maternal investment are expected to improve survival and reproduction. In mammals, maternal investment via lactation predicts offspring growth. As body mass is often associated with fitness consequences, females have the potential to influence offspring fitness through their level of investment, which might interact with effects of population density and temperature. Here, we investigate the relationship between pup body mass at day 13 (used as approximation for weaning mass) and individual reproductive parameters as well as longevity under natural variation in population density and temperatures. Further, we assess the extent to which mothers influence the body mass of their offspring until weaning. We analysed life data of 384 house mice (Mus musculus domesticus) from a free-living wild population that was not food limited. We found a complex effect of population density, temperature and maternal investment on life-history traits related to fitness: Shorter longevity with increasing pup body mass at day 13; delayed reproduction of heavier pups when raised at warmer temperatures; and increased lifetime reproductive success for heavier pups at high densities. House mice could use population density and temperature as cues for predicting future environmental conditions, allowing a mother to adjust her investment according to the environment in which offspring will breed in order to maximise fitness. This study highlights the importance of considering ecological conditions in combination with maternal effects.


2019 ◽  
Vol 116 (18) ◽  
pp. 8919-8924 ◽  
Author(s):  
Eli D. Strauss ◽  
Kay E. Holekamp

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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