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Maternal investment, life histories, and the costs of brain growth in mammals.

ABSTRACT: Brain size variation in mammals correlates with life histories: larger-brained species have longer gestations, mature later, and have increased lifespans. These patterns have been explained in terms of developmental costs (larger brains take longer to grow) and cognitive benefits (large brains enhance survival and increase lifespan). In support of the developmental cost hypothesis, we show that evolutionary changes in pre- and postnatal brain growth correlate specifically with duration of the relevant phases of maternal investment (gestation and lactation, respectively). We also find support for the hypothesis that the rate of fetal brain growth is related to the energy turnover of the mother. In contrast, we find no support for hypotheses proposing that costs are accommodated through direct tradeoffs between brain and body growth, or between brain growth and litter size. When the duration of maternal investment is taken into account, adult brain size is uncorrelated with other life history traits such as lifespan. Hence, the general pattern of slower life histories in large-brained species appears to be a direct consequence of developmental costs.

SUBMITTER: Barton RA

PROVIDER: S-EPMC3076843 | biostudies-other | 2011 Apr

REPOSITORIES: biostudies-other

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Maternal investment, life histories, and the costs of brain growth in mammals.

Barton Robert A RA Capellini Isabella I

Proceedings of the National Academy of Sciences of the United States of America 20110328 15

Brain size variation in mammals correlates with life histories: larger-brained species have longer gestations, mature later, and have increased lifespans. These patterns have been explained in terms of developmental costs (larger brains take longer to grow) and cognitive benefits (large brains enhance survival and increase lifespan). In support of the developmental cost hypothesis, we show that evolutionary changes in pre- and postnatal brain growth correlate specifically with duration of the re ...[more]

PMID: 21444808

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Project description: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.

Project description:IntroductionMaternal capital (MC) is a broad term from evolutionary biology, referring to any aspects of maternal phenotype that represent resources available for investment in offspring. We investigated MC in breastfeeding mothers of late preterm and early term infants, examining its relationship with infant and breastfeeding outcomes. We also determined whether MC modified the effect of the relaxation intervention on these outcomes.MethodsThe data was collected as part of a randomized controlled trial investigating breastfeeding relaxation in 72 mothers of late preterm and early term infants. Indicators of MC (socioeconomic, social, somatic, reproductive, psychological, and cognitive) were collected at baseline at 2-3 weeks post-delivery. Principal Component Analysis was conducted for the MC measures and two components were identified: 1."Subjective" maternal capital which included stress and depression scores, and 2."Objective" maternal capital which included height, infant birth weight, and verbal memory. Univariate linear regression was conducted to assess the relationship between objective and subjective MC (predictors) and infant growth, infant behavior, maternal behavior, and infant feeding variables (outcomes) at 6-8 weeks. The interaction of MC and intervention assignment with outcomes was assessed.ResultsHigher objective MC was significantly associated with higher infant weight (0.43; 95%CI 0.21,0.66) and length z-scores (0.47; 95%CI 0.19,0.76), shorter duration of crying (-17.5; 95%CI -33.2,-1.9), and lower food (-0.28; 95%CI -0.48,-0.08) and satiety responsiveness (-0.17; 95%CI -0.31,-0.02) at 6-8 weeks. It was also associated with greater maternal responsiveness to infant cues (-0.05, 95%CI -0.09,-0.02 for non-responsiveness). Greater subjective maternal capital was significantly associated with higher breastfeeding frequency (2.3; 95%CI 0.8,3.8) and infant appetite (0.30; 95%CI 0.07,0.54). There was a significant interaction between the intervention assignment and objective MC for infant length, with trends for infant weight and crying, which indicated that the intervention had greater effects among mothers with lower capital.ConclusionHigher MC was associated with better infant growth and shorter crying duration. This was possibly mediated through more frequent breastfeeding and prompt responsiveness to infant cues, reflecting greater maternal investment. The findings also suggest that a relaxation intervention was most effective among those with low MC, suggesting some reduction in social inequalities in health.

Project description:For 40 years, paleontological studies of marine gastropods have suggested that species selection favors lineages with short-lived (lecithotrophic) larvae, which are less dispersive than long-lived (planktotrophic) larvae. Although lecithotrophs appeared to speciate more often and accumulate over time in some groups, lecithotrophy also increased extinction rates, and tests for state-dependent diversification were never performed. Molecular phylogenies of diverse groups instead suggested lecithotrophs accumulate without diversifying due to frequent, unidirectional character change. Although lecithotrophy has repeatedly originated in most phyla, no adult trait has been correlated with shifts in larval type. Thus, both the evolutionary origins of lecithotrophy and its consequences for patterns of species richness remain poorly understood. Here, we test hypothesized links between development mode and evolutionary rates using likelihood-based methods and a phylogeny of 202 species of gastropod molluscs in Sacoglossa, a clade of herbivorous sea slugs. Evolutionary quantitative genetics modeling and stochastic character mapping supported 27 origins of lecithotrophy. Tests for correlated evolution revealed lecithotrophy evolved more often in lineages investing in extra-embryonic yolk, the first adult trait associated with shifts in development mode across a group. However, contrary to predictions from paleontological studies, species selection actually favored planktotrophy; most extant lecithotrophs originated through recent character change, and did not subsequently diversify. Increased offspring provisioning in planktotrophs thus favored shifts to short-lived larvae, which led to short-lived lineages over macroevolutionary time scales. These findings challenge long-standing assumptions about the effects of alternative life histories in the sea. Species selection can explain the long-term persistence of planktotrophy, the ancestral state in most clades, despite frequent transitions to lecithotrophy.

Dataset Information

Maternal investment, life histories, and the costs of brain growth in mammals.

Publications

Maternal investment, life histories, and the costs of brain growth in mammals.

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