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

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.

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.


2005 ◽  
Vol 273 (1587) ◽  
pp. 741-750 ◽  
Author(s):  
Barbara Taborsky

There is increasing evidence that the environment experienced early in life can strongly influence adult life histories. It is largely unknown, however, how past and present conditions influence suites of life-history traits regarding major life-history trade-offs. Especially in animals with indeterminate growth, we may expect that environmental conditions of juveniles and adults independently or interactively influence the life-history trade-off between growth and reproduction after maturation. Juvenile growth conditions may initiate a feedback loop determining adult allocation patterns, triggered by size-dependent mortality risk. I tested this possibility in a long-term growth experiment with mouthbrooding cichlids. Females were raised either on a high-food or low-food diet. After maturation half of them were switched to the opposite treatment, while the other half remained unchanged. Adult growth was determined by current resource availability, but key reproductive traits like reproductive rate and offspring size were only influenced by juvenile growth conditions, irrespective of the ration received as adults. Moreover, the allocation of resources to growth versus reproduction and to offspring number versus size were shaped by juvenile rather than adult ecology. These results indicate that early individual history must be considered when analysing causes of life-history variation in natural populations.


1939 ◽  
Vol 59 (3) ◽  
pp. 563-597 ◽  
Author(s):  
Robert Carrick

Among Gasteropod Molluscs the life-histories and development of the most highly evolved members, the terrestrial Pulmonates, have been less intensively studied than those of more primitive aquatic forms. This has been due in part to the technical difficulties involved in the permanent preparation of material for study, and in part to the fact that the investigator seeking for primitive features of phyletic interest is more likely to find these among more generalised species of Gasteropods than among those which are obviously adapted, both during the early stages of their development and in adult life, to a habitat far removed from the ancestral one.It is the purpose of this paper to present data bearing upon the life-history of a single species of land Pulmonate, Agriolimax agrestis L., to enlarge upon certain aspects of the embryology of this species, and to demonstrate the structural and functional changes of the larva which have accompanied the transition from an aquatic to a terrestrial breeding habit.


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.


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.


2016 ◽  
Vol 371 (1690) ◽  
pp. 20150187 ◽  
Author(s):  
Daniel Sol ◽  
Ferran Sayol ◽  
Simon Ducatez ◽  
Louis Lefebvre

The evolutionary origin of innovativeness remains puzzling because innovating means responding to novel or unusual problems and hence is unlikely to be selected by itself. A plausible alternative is considering innovativeness as a co-opted product of traits that have evolved for other functions yet together predispose individuals to solve problems by adopting novel behaviours. However, this raises the question of why these adaptations should evolve together in an animal. Here, we develop the argument that the adaptations enabling animals to innovate evolve together because they are jointly part of a life-history strategy for coping with environmental changes. In support of this claim, we present comparative evidence showing that in birds, (i) innovative propensity is linked to life histories that prioritize future over current reproduction, (ii) the link is in part explained by differences in brain size, and (iii) innovative propensity and life-history traits may evolve together in generalist species that frequently expose themselves to novel or unusual conditions. Combined with previous evidence, these findings suggest that innovativeness is not a specialized adaptation but more likely part of a broader general adaptive system to cope with changes in the environment.


2015 ◽  
Vol 85 (1) ◽  
pp. 63-76 ◽  
Author(s):  
Iulian Ilieş ◽  
Mario L. Muscedere ◽  
James F.A. Traniello

A central question in brain evolution concerns how selection has structured neuromorphological variation to generate adaptive behavior. In social insects, brain structures differ between reproductive and sterile castes, and worker behavioral specializations related to morphology, age, and ecology are associated with intra- and interspecific variation in investment in functionally different brain compartments. Workers in the hyperdiverse ant genus Pheidole are morphologically and behaviorally differentiated into minor and major subcastes that exhibit distinct species-typical patterns of brain compartment size variation. We examined integration and modularity in brain organization and its developmental patterning in three ecotypical Pheidole species by analyzing intra- and interspecific morphological and neuroanatomical covariation. Our results identified two trait clusters, the first involving olfaction and social information processing and the second composed of brain regions regulating nonolfactory sensorimotor functions. Patterns of size covariation between brain compartments within subcastes were consistent with levels of behavioral differentiation between minor and major workers. Globally, brains of mature workers were more heterogeneous than brains of newly eclosed workers, suggesting diversified developmental trajectories underscore species- and subcaste-typical brain organization. Variation in brain structure associated with the striking worker polyphenism in our sample of Pheidole appears to originate from initially differentiated brain templates that further diverge through species- and subcaste-specific processes of maturation and behavioral development.


PLoS ONE ◽  
2021 ◽  
Vol 16 (12) ◽  
pp. e0261185
Author(s):  
Helen Rebecca Chambers ◽  
Sandra Andrea Heldstab ◽  
Sean J. O’Hara

Despite decades of research, much uncertainty remains regarding the selection pressures responsible for brain size variation. Whilst the influential social brain hypothesis once garnered extensive support, more recent studies have failed to find support for a link between brain size and sociality. Instead, it appears there is now substantial evidence suggesting ecology better predicts brain size in both primates and carnivores. Here, different models of brain evolution were tested, and the relative importance of social, ecological, and life-history traits were assessed on both overall encephalisation and specific brain regions. In primates, evidence is found for consistent associations between brain size and ecological factors, particularly diet; however, evidence was also found advocating sociality as a selection pressure driving brain size. In carnivores, evidence suggests ecological variables, most notably home range size, are influencing brain size; whereas, no support is found for the social brain hypothesis, perhaps reflecting the fact sociality appears to be limited to a select few taxa. Life-history associations reveal complex selection mechanisms to be counterbalancing the costs associated with expensive brain tissue through extended developmental periods, reduced fertility, and extended maximum lifespan. Future studies should give careful consideration of the methods chosen for measuring brain size, investigate both whole brain and specific brain regions where possible, and look to integrate multiple variables, thus fully capturing all of the potential factors influencing brain size.


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