Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.
The prolonged juvenile period exhibited by primates is an evolutionary conundrum. Here we examine wild chimpanzee feeding development in the context of two hypotheses regarding prolonged development in primates: the needing‐to‐learn hypothesis and the expensive brain hypothesis.
We studied wild chimpanzee (
Feeding time, diet breadth, and diet maturity exhibited the most substantial increases with age in the first 6 years, with no significant change thereafter. Males and females showed different patterns of change in diet breadth by age, but did not differ by age 10. Diet composition did not change significantly with age and did not differ by sex.
We found that chimpanzee offspring attained adult‐like feeding behaviors between 4 and 6 years of age, concomitant with the completion of weaning. Thus, our data do not support the needing‐to‐learn feeding skills hypothesis of a prolonged juvenile period, but additional data are needed to evaluate how and when adolescent chimpanzees are able to make foraging decisions independent of their mothers. Existing data on growth provides support for the expensive brain hypothesis, however, these hypotheses are not necessarily mutually exclusive. As more studies across taxa accumulate sufficient datasets on a range of developmental metrics, we will be able to achieve a more robust understanding of prolonged development in primates.
- Award ID(s):
- 1753437
- NSF-PAR ID:
- 10452926
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- American Journal of Physical Anthropology
- Volume:
- 175
- Issue:
- 1
- ISSN:
- 0002-9483
- Format(s):
- Medium: X Size: p. 268-281
- Size(s):
- ["p. 268-281"]
- Sponsoring Org:
- National Science Foundation
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Abstract Many ectotherms rely on temperature cues experienced during development to determine offspring sex. The first descriptions of temperature‐dependent sex determination (TSD) were made over 50 years ago, yet an understanding of its adaptive significance remains elusive, especially in long‐lived taxa.
One novel hypothesis predicts that TSD should be evolutionarily favoured when two criteria are met—(a) incubation temperature influences annual juvenile survival and (b) sexes mature at different ages. Under these conditions, a sex‐dependent effect of incubation temperature on offspring fitness arises through differences in age at sexual maturity, with the sex that matures later benefiting disproportionately from temperatures that promote juvenile survival.
The American alligator (
Alligator mississippiensis ) serves as an insightful model in which to test this hypothesis, as males begin reproducing nearly a decade after females. Here, through a combination of artificial incubation experiments and mark‐recapture approaches, we test the specific predictions of the survival‐to‐maturity hypothesis for the adaptive value of TSD by disentangling the effects of incubation temperature and sex on annual survival of alligator hatchlings across two geographically distinct sites.Hatchlings incubated at male‐promoting temperatures (MPTs) consistently exhibited higher survival compared to those incubated at female‐promoting temperatures. This pattern appears independent of hatchling sex, as females produced from hormone manipulation at MPT exhibit similar survival to their male counterparts.
Additional experiments show that incubation temperature may affect early‐life survival primarily by affecting the efficiency with which maternally transferred energy resources are used during development.
Results from this study provide the first explicit empirical support for the adaptive value of TSD in a crocodilian and point to developmental energetics as a potential unifying mechanism underlying persistent survival consequences of incubation temperature.
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Life history and socioecological factors have been linked to species‐specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method—parallel lasers—to examine shoulder‐rump (SR) growth in a wild primate, the gelada (
Theropithecus gelada , Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size‐for‐age patterns (N = 154 females;N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably “cheap,” neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707–719, 2016. © 2016 Wiley Periodicals, Inc. -
For species with low mortality and high reproductive costs, like primates, rather than maximize reproduction, natural selection should favor slow growth and slow reproductive rates. Orangutans, because of their slow life history, and the extreme fluctuations in their food supply, are hypothesized to have been selected for slow juvenile development to avoid ecological risk. Juveniles are predicted to be particularly vulnerable during periods of low food availability because of lower foraging success. Thus, we tested the hypothesis that juvenile orangutans are less efficient foragers than adults and that they are less able to both access and digest important fall-back foods. Data were collected on wild orangutans in Gunung Palung National Park, Borneo, Indonesia between 1994-2016. Analyses are drawn from 468 matched follows of mother-offspring pairs in which more than 75% of the diet has been analyzed. We found that juveniles ate fruit when their mother’s ate fruit during 98.3% of bouts. However, for other food items, juveniles were much less likely to eat the same food items (insects = 65.2%, leaves 76.5, bark 70.0%, flowers 75.0%, pith 65.8%). As expected, we found that juveniles ate significantly fewer calories than did adults overall, but this difference was particularly pronounced during periods of low food availability (p < 0.001). We show that these results were due to constraints on both the processing and digesting of fall-back foods. Thus, the long period of orangutan growth and dependency may reflect a risk-averse growth strategy in this forest characterized by dramatic fluctuations in preferred fruits.more » « less
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For species with low mortality and high reproductive costs, like primates, rather than maximize reproduction, natural selection should favor slow growth and slow reproductive rates. Orangutans, because of their slow life history, and the extreme fluctuations in their food supply, are hypothesized to have been selected for slow juvenile development to avoid ecological risk. Juveniles are predicted to be particularly vulnerable during periods of low food availability because of lower foraging success. Thus, we tested the hypothesis that juvenile orangutans are less efficient foragers than adults and that they are less able to both access and digest important fall-back foods. Data were collected on wild orangutans in Gunung Palung National Park, Borneo, Indonesia between 1994-2016. Analyses are drawn from 468 matched follows of mother-offspring pairs in which more than 75% of the diet has been analyzed. We found that juveniles ate fruit when their mother’s ate fruit during 98.3% of bouts. However, for other food items, juveniles were much less likely to eat the same food items (insects = 65.2%, leaves 76.5, bark 70.0%, flowers 75.0%, pith 65.8%). As expected, we found that juveniles ate significantly fewer calories than did adults overall, but this difference was particularly pronounced during periods of low food availability (p < 0.001). We show that these results were due to constraints on both the processing and digesting of fall-back foods. Thus, the long period of orangutan growth and dependency may reflect a risk-averse growth strategy in this forest characterized by dramatic fluctuations in preferred fruits.more » « less
