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Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

ABSTRACT: Background:In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chimpanzees, offspring are typically weaned at approximately 4?years old, yet immature individuals continue to associate with their mothers for up to 10?years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear.The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15?years. Results:We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. Conclusion:Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

SUBMITTER: Samuni L

PROVIDER: S-EPMC6945487 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (<i>Pan troglodytes verus</i>).

Samuni Liran L Tkaczynski Patrick P Deschner Tobias T Löhrrich Therese T Wittig Roman M RM Crockford Catherine C

Frontiers in zoology 20200107

<h4>Background</h4>In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chim ...[more]

PMID: 31911809

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Project description:Compared to great apes, humans maintain a relatively rapid reproductive pace despite long periods of dependency. This seemingly contradictory set of traits is made possible by weaning offspring before nutritional independence and alloparents who help provide care. In traditional societies, this help may be provided to mothers in part by their juvenile offspring who carry, supervise, or provision younger siblings. In contrast to humans, chimpanzees (Pan troglodytes) are nutritionally independent after weaning, yet juveniles continue to travel with their mother and younger sibling for an additional 4-5 years. This continued association could be costly to the mother if she continues to invest in weaned offspring. Alternately, while juvenile chimpanzees do not typically provision younger siblings, their presence and social interaction with infants may allow mothers to focus on other tasks. In this study, we investigate the costs and benefits to mothers of continued association with juveniles in wild chimpanzees. Using 26 years of long-term behavioral data we examined how maternal activity budgets varied based on the presence of a dependent juvenile offspring. We found that continued social interaction between mothers and juveniles does not influence the mother's time allocated to interacting with the younger infant, her feeding, resting, or travel time, or time socializing with other community members. Instead, mothers may benefit from the additional social interaction and/or relationship with their older offspring. Using 45 years of demographic data we found that those offspring who had an older sibling tended to be more likely to survive each year from birth to 8 years than those without an older sibling. Additionally, interbirth intervals were more likely to end when the female had an older offspring present. A mutually beneficial mother-juvenile dynamic in great apes provides insight into continued association between mothers and offspring after nutritional independence and the emergence of juvenile helping during hominin evolution.

Project description:BackgroundMany species are threatened with extinction as their population sizes decrease with changing environments or face novel pathogenic threats. A reduction of genetic diversity at major histocompatibility complex (MHC) genes may have dramatic effects on populations' survival, as these genes play a key role in adaptive immunity. This might be the case for chimpanzees, the MHC genes of which reveal signatures of an ancient selective sweep likely due to a viral epidemic that reduced their population size a few million years ago. To better assess how this past event affected MHC variation in chimpanzees compared to humans, we analysed several indexes of genetic diversity and linkage disequilibrium across seven MHC genes on four cohorts of chimpanzees and we compared them to those estimated at orthologous HLA genes in a large set of human populations.ResultsInterestingly, the analyses uncovered similar patterns of both molecular diversity and linkage disequilibrium across the seven MHC genes in chimpanzees and humans. Indeed, in both species the greatest allelic richness and heterozygosity were found at loci A, B, C and DRB1, the greatest nucleotide diversity at loci DRB1, DQA1 and DQB1, and both significant global linkage disequilibrium and the greatest proportions of haplotypes in linkage disequilibrium were observed at pairs DQA1?~?DQB1, DQA1?~?DRB1, DQB1?~?DRB1 and B?~?C. Our results also showed that, despite some differences among loci, the levels of genetic diversity and linkage disequilibrium observed in contemporary chimpanzees were globally similar to those estimated in small isolated human populations, in contrast to significant differences compared to large populations.ConclusionsWe conclude, first, that highly conserved mechanisms shaped the diversity of orthologous MHC genes in chimpanzees and humans. Furthermore, our findings support the hypothesis that an ancient demographic decline affecting the chimpanzee populations - like that ascribed to a viral epidemic - exerted a substantial effect on the molecular diversity of their MHC genes, albeit not more pronounced than that experienced by HLA genes in human populations that underwent rapid genetic drift during humans' peopling history. We thus propose a model where chimpanzees' MHC genes regenerated molecular variation through recombination/gene conversion and/or balancing selection after the selective sweep.

Dataset Information

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

Publications

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (<i>Pan troglodytes verus</i>).

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