Maternal investment, life histories and the evolution of brain structure in primates

Abstract

Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

Systematic mapping of developmental milestones in wild chimpanzees

“…However, overall our findings are in line with the delayed benefits hypothesis, which posits that extended development is necessary for acquiring adult skills, with these skills being linked to increases in overall survival and fitness, and therefore leading to the selection of similar life histories in humans and chimpanzees (Charnov & Berrigan, 1993;Jones, 2011;Powell et al, 2019;Stearns, 1992).…”

“…Overall, we found that developmental milestones continue to emerge at least across the first 5 years of chimpanzee life. We found no general bias of earlier development compared to humans, supporting the delayed benefits hypothesis (Charnov & Berrigan, 1993; Jones, 2011; Powell et al, 2019; Stearns, 1992). Particularly, more complex traits such as fine motor, social interaction and communication traits generally emerged later than gross motor milestones with considerable variation between individuals.…”

“…In contrast, intentionality in chimpanzees has largely been demonstrated in adults (Crockford, Wittig, Mundry, & Zuberbühler, 2012; Crockford, Wittig, & Zuberbühler, 2015; Hobaiter & Byrne, 2014; Schel, Townsend, Machanda, Zuberbühler, & Slocombe, 2013), and it is not yet known when this complex form of social cognition develops in the species. However, overall our findings are in line with the delayed benefits hypothesis, which posits that extended development is necessary for acquiring adult skills, with these skills being linked to increases in overall survival and fitness, and therefore leading to the selection of similar life histories in humans and chimpanzees (Charnov & Berrigan, 1993; Jones, 2011; Powell et al., 2019; Stearns, 1992).…”

“…Overall, we found that developmental milestones continue to emerge at least across the first 5 years of chimpanzee life. We found no general bias of earlier development compared to humans, supporting the delayed benefits hypothesis (Charnov & Berrigan, 1993;Jones, 2011;Powell et al, 2019;Stearns, 1992).…”

“…prenatal maternal constraints such as the obstetrical dilemma hypothesis Rosenberg & Trevathan, 1995; Washburn, 1960) or the metabolic dilemma hypothesis (Dunsworth, Warrener, Deacon, Ellison, & Pontzer, 2012), or by a necessity to acquire relevant skills for adult survival (e.g. the delayed benefits hypothesis, Powell, Barton, & Street, 2019).…”