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

2019 ◽  
Author(s):  
Lauren E Powell ◽  
Sally E Street ◽  
Robert A Barton

AbstractLife history is a robust correlate of relative brain size: large-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. One influential adaptive hypothesis to account for this finding is the Cognitive Buffer Hypothesis (CBH). The CBH proposes that large brains permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing reduced mortality and increased lifespan. In 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. The hypotheses are not mutually exclusive but do make different predictions. Here we test novel predictions of the hypotheses in primates: examining how the volume of brain components with different developmental trajectories correlate with relevant phases of maternal investment, juvenile period and post-maturational lifespan. Consistent with the DCH, structures with different allocations of growth to pre-natal versus post-natal development exhibit predictably divergent correlations with the associated periods of maternal investment and pre-maturational lifespan. Contrary to the CBH, adult lifespan is uncorrelated with either whole brain size or the size of individual brain components once duration of maternal investment is accounted for. 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 mechanisms, and imply that postnatal maturational processes involving interaction with the environment may be particularly crucial for the development of cerebellar function. They also provide an explanation for why apes have relatively extended maturation times, which relate to the relative expansion of the cerebellum in this clade.

2019 ◽  
Vol 286 (1911) ◽  
pp. 20191608 ◽  
Author(s):  
Lauren E. Powell ◽  
Robert A. Barton ◽  
Sally E. Street

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.


Author(s):  
Barbara L. Finlay

Understanding the adaptive functions of increasing brain size have occupied scientists for decades. Here, taking the general perspective of the Extended Evolutionary Synthesis, the question of how brains change in size will be considered in two developmental frameworks. The first framework will consider the particular developmental mechanisms that control and generate brain mass, concentrating on neurogenesis in a comparative vertebrate context. The consequences of limited adult neurogenesis in mammals, and the dominating role of duration of neurogenesis for mammalian evolution will be discussed for the particular case of the teleost versus mammalian retina, and for paths of brain evolution more generally. The second framework examines brain mass in terms of life history, particularly the features of life history that correlate highly, if imperfectly, with brain mass, including duration of development to adolescence, duration of parental care, body and range size, and longevity. This covariation will be examined in light of current work on genetic causes and consequences of covariation in craniofacial bone groupings. The eventual development of a multivariate structure for understanding brain evolution which specifically integrates formerly separate layers of analysis is the ultimate goal.


Author(s):  
Maren N. Vitousek ◽  
Laura A. Schoenle

Hormones mediate the expression of life history traits—phenotypic traits that contribute to lifetime fitness (i.e., reproductive timing, growth rate, number and size of offspring). The endocrine system shapes phenotype by organizing tissues during developmental periods and by activating changes in behavior, physiology, and morphology in response to varying physical and social environments. Because hormones can simultaneously regulate many traits (hormonal pleiotropy), they are important mediators of life history trade-offs among growth, reproduction, and survival. This chapter reviews the role of hormones in shaping life histories with an emphasis on developmental plasticity and reversible flexibility in endocrine and life history traits. It also discusses the advantages of studying hormone–behavior interactions from an evolutionary perspective. Recent research in evolutionary endocrinology has provided insight into the heritability of endocrine traits, how selection on hormone systems may influence the evolution of life histories, and the role of hormonal pleiotropy in driving or constraining evolution.


2020 ◽  
Vol 375 (1803) ◽  
pp. 20190495 ◽  
Author(s):  
Natalie Uomini ◽  
Joanna Fairlie ◽  
Russell D. Gray ◽  
Michael Griesser

Traditional attempts to understand the evolution of human cognition compare humans with other primates. This research showed that relative brain size covaries with cognitive skills, while adaptations that buffer the developmental and energetic costs of large brains (e.g. allomaternal care), and ecological or social benefits of cognitive abilities, are critical for their evolution. To understand the drivers of cognitive adaptations, it is profitable to consider distant lineages with convergently evolved cognitions. Here, we examine the facilitators of cognitive evolution in corvid birds, where some species display cultural learning, with an emphasis on family life. We propose that extended parenting (protracted parent–offspring association) is pivotal in the evolution of cognition: it combines critical life-history, social and ecological conditions allowing for the development and maintenance of cognitive skillsets that confer fitness benefits to individuals. This novel hypothesis complements the extended childhood idea by considering the parents' role in juvenile development. Using phylogenetic comparative analyses, we show that corvids have larger body sizes, longer development times, extended parenting and larger relative brain sizes than other passerines. Case studies from two corvid species with different ecologies and social systems highlight the critical role of life-history features on juveniles’ cognitive development: extended parenting provides a safe haven, access to tolerant role models, reliable learning opportunities and food, resulting in higher survival. The benefits of extended juvenile learning periods, over evolutionary time, lead to selection for expanded cognitive skillsets. Similarly, in our ancestors, cooperative breeding and increased group sizes facilitated learning and teaching. Our analyses highlight the critical role of life-history, ecological and social factors that underlie both extended parenting and expanded cognitive skillsets. This article is part of the theme issue ‘Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals’.


Author(s):  
Ken H. Andersen

This chapter develops descriptions of how individuals grow and reproduce. More specifically, the chapter seeks to determine the growth and reproduction rates from the consumption rate, by developing an energy budget of the individual as a function of size. To that end, the chapter addresses the question of how an individual makes use of the energy acquired from consumption. It sets up the energy budgets of individuals by formulating the growth model using so-called life-history invariants, which are parameters that do not vary systematically between species. While the formulation of the growth model in terms of life-history invariants is largely successful, there is in particular one parameter that is not invariant between life histories: the asymptotic size (maximum size) of individuals in the population. This parameter plays the role of a master trait that characterizes most of the variation between life histories.


2010 ◽  
Vol 67 (4) ◽  
pp. 720-729 ◽  
Author(s):  
Amina E. Price ◽  
Paul Humphries

This study investigated the importance of dispersal and retention processes during early ontogeny for three caridean shrimp species that complete their entire life history in freshwater. Directional traps were used to examine the small-scale movement patterns of shrimp into and out of nursery habitat patches (slackwaters) in a small lowland river in southeastern Australia. Movement patterns provided evidence for two contrasting life history based dispersal and retention strategies. For the two smaller atyid species, Paratya australiensis and Caridina mccullochi , the majority of larvae remained within the slackwater in which they were hatched until the final stage of development, at which point dispersal, either among slackwaters or out of slackwaters to faster-flowing pool and run habitats, occurred. For the larger palaemonid species, Macrobrachium australiense , larvae were hatched into slackwaters and dispersal occurred predominately during the first stage of larval development and then decreased as development progressed. Despite the differences in dispersal strategies among species, movement was mostly associated with a particular larval stage and thus emphasizes the importance of retention during critical developmental periods and of the potential impact that flow alteration could have on these and other species with similar life histories.


2019 ◽  
Vol 93 (1) ◽  
pp. 4-18 ◽  
Author(s):  
J. Frances Kamhi ◽  
Iulian Ilieş ◽  
James F.A. Traniello

The behavioral demands of living in social groups have been linked to the evolution of brain size and structure, but how social organization shapes investment and connectivity within and among functionally specialized brain regions remains unclear. To understand the influence of sociality on brain evolution in ants, a premier clade of eusocial insects, we statistically analyzed patterns of brain region size covariation as a proxy for brain region connectivity. We investigated brain structure covariance in young and old workers of two formicine ants, the Australasian weaver ant Oecophylla smaragdina, a pinnacle of social complexity in insects, and its socially basic sister clade Formica subsericea. As previously identified in other ant species, we predicted that our analysis would recognize in both species an olfaction-related brain module underpinning social information processing in the brain, and a second neuroanatomical cluster involved in nonolfactory sensorimotor processes, thus reflecting conservation of compartmental connectivity. Furthermore, we hypothesized that covariance patterns would reflect divergence in social organization and life histories either within this species pair or compared to other ant species. Contrary to our predictions, our covariance analyses revealed a weakly defined visual, rather than olfactory, sensory processing cluster in both species. This pattern may be linked to the reliance on vision for worker behavioral performance outside of the nest and the correlated expansion of the optic lobes to meet navigational demands in both species. Additionally, we found that colony size and social organization, key measures of social complexity, were only weakly correlated with brain modularity in these formicine ants. Worker age also contributed to variance in brain organization, though in different ways in each species. These findings suggest that brain organization may be shaped by the divergent life histories of the two study species. We compare our findings with patterns of brain organization of other eusocial insects.


2007 ◽  
Vol 362 (1480) ◽  
pp. 649-658 ◽  
Author(s):  
R.I.M Dunbar ◽  
Susanne Shultz

We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for ‘software’ programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se ; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.


2016 ◽  
Vol 30 (1) ◽  
pp. 150-160 ◽  
Author(s):  
M. Tsuboi ◽  
A. C. O. Lim ◽  
B. L. Ooi ◽  
M. Y. Yip ◽  
V. C. Chong ◽  
...  

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