The human brain is unusually large. It has tripled in size from Australopithecines to modern humans and has become almost six times larger than expected for a placental mammal of human size . Brains incur high metabolic costs and accordingly a long-standing question is why the large human brain has evolved . The leading hypotheses propose benefits of improved cognition for overcoming ecological, social or cultural challenges. However, these hypotheses are typically assessed using correlative analyses, and establishing causes for brain-size evolution remains difficult. Here we introduce a metabolic approach that enables causal assessment of social hypotheses for brain-size evolution. Our approach yields quantitative predictions for brain and body size from formalized social hypotheses given empirical estimates of the metabolic costs of the brain. Our model predicts the evolution of adult Homo sapiens-sized brains and bodies when individuals face a combination of 60% ecological, 30% cooperative and 10% between-group competitive challenges, and suggests that between-individual competition has been unimportant for driving human brain-size evolution. Moreover, our model indicates that brain expansion in Homo was driven by ecological rather than social challenges, and was perhaps strongly promoted by culture. Our metabolic approach thus enables causal assessments that refine, refute and unify hypotheses of brain-size evolution.
Natural selection acts on phenotypes constructed over development, which raises the question of how development affects evolution. Existing mathematical theory has considered either evolutionary dynamics while neglecting developmental dynamics, or developmental dynamics while neglecting evolutionary dynamics by assuming evolutionary equilibrium. We formulate a mathematical framework that integrates explicit developmental dynamics into evolutionary dynamics. We consider two types of traits: genetic traits called control variables and developed traits called state variables. Developed traits are constructed over ontogeny according to a developmental map of ontogenetically prior traits and the social and non-social environment. We obtain general equations describing the evolutionary-developmental (evo-devo) dynamics. These equations can be arranged in a layered structure called the evo-devo process, where five elementary components generate all equations including those describing genetic covariation and the evo-devo dynamics. These equations recover Lande's equation as a special case and describe the evolution of Lande's G-matrix from the evolution of the phenotype, environment, and mutational covariation. This shows that genetic variation is necessarily absent in some directions of phenotype space if at least one trait develops and enough traits are included in the analysis so as to guarantee dynamic sufficiency. Consequently, directional selection alone is generally insufficient to identify evolutionary equilibria. Instead, "total genetic selection" is sufficient to identify evolutionary equilibria if mutational variation exists in all directions of control space and exogenous plastic response vanishes. Developmental and environmental constraints influence the evolutionary equilibria and determine the admissible evolutionary trajectory. These results show that development has major evolutionary effects.
Many social behaviors are triggered by social partners. For example, cells in a multicellular organism often become soma via extrinsically regulated differentiation, while individuals in a eusocial colony often become helpers via extrinsic caste determination. One explanation for social triggering is that it informs when it is beneficial to express the behavior. Alternatively, social triggering can represent manipulation where social partners partially or completely control the focal individual's behavior. For instance, caste determination in primitively eusocial taxa is typically accomplished via differential feeding or dominance hierarchies, suggesting some manipulation. However, selection would favor resistance if manipulation is detrimental to manipulated parties, and the outcome of the manipulation conflict remains intricate. We analyze the coevolution of manipulation and resistance in a simple but general setting. We show that, despite possible resistance, manipulated behavior can be established under less stringent conditions than spontaneous (i.e., nonmanipulated) behavior because of resistance costs. The existence of this advantage might explain why primitive eusocial behavior tends to be triggered socially and coercively. We provide a simple condition for the advantage of manipulated behavior that may help infer whether a socially triggered behavior is manipulated. We illustrate our analysis with a hypothetical example of maternal manipulation relevant to primitive eusociality.
Complex cognition and relatively large brains are distributed across various taxa, and many primarily verbal hypotheses exist to explain such diversity. Yet, mathematical approaches formalizing verbal hypotheses would help deepen the understanding of brain and cognition evolution. With this aim, we combine elements of life history and metabolic theories to formulate a metabolically explicit mathematical model for brain life history evolution. We assume that some of the brain’s energetic expense is due to production (learning) and maintenance (memory) of energy-extraction skills (or cognitive abilities, knowledge, information, etc.). We also assume that individuals use such skills to extract energy from the environment, and can allocate this energy to grow and maintain the body, including brain and reproductive tissues. The model can be used to ask what fraction of growth energy should be allocated at each age, given natural selection, to growing brain and other tissues under various biological settings. We apply the model to find uninvadable allocation strategies under a baseline setting (“me vs nature”), namely when energy-extraction challenges are environmentally determined and are overcome individually but possibly with maternal help, and use modern-human data to estimate model’s parameter values. The resulting uninvadable strategies yield predictions for brain and body mass throughout ontogeny and for the ages at maturity, adulthood, and brain growth arrest. We find that: (1) a me-vs-nature setting is enough to generate adult brain and body mass of ancient human scale and a sequence of childhood, adolescence, and adulthood stages; (2) large brains are favored by intermediately challenging environments, moderately effective skills, and metabolically expensive memory; and (3) adult skill is proportional to brain mass when metabolic costs of memory saturate the brain metabolic rate allocated to skills.
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