The multiple contexts of brain scaling: Phenotypic integration in brain and behavioral evolution

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.

Scaffolding layered control architectures through constraint closure: insights into brain evolution and development

The functional organization of the mammalian brain can be considered to form a layered control architecture, but how this complex system has emerged through evolution and is constructed during development remains a puzzle. Here we consider brain organization through the framework of constraint closure, viewed as a general characteristic of living systems, that they are composed of multiple sub-systems that constrain each other at different timescales. We do so by developing a new formalism for constraint closure, inspired by a previous model showing how within-lifetime dynamics can constrain between-lifetime dynamics, and we demonstrate how this interaction can be generalized to multi-layered systems. Through this model, we consider brain organization in the context of two major examples of constraint closure—physiological regulation and visual orienting. Our analysis draws attention to the capacity of layered brain architectures to scaffold themselves across multiple timescales, including the ability of cortical processes to constrain the evolution of sub-cortical processes, and of the latter to constrain the space in which cortical systems self-organize and refine themselves. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Species-specific mitochondria dynamics and metabolism regulate the timing of neuronal development.

The evolution of species involves changes in the timeline of key developmental programs. Among these, neuronal development is considerably prolonged in the human cerebral cortex compared with other mammals, leading to brain neoteny. Here we explore whether mitochondria influence the species-specific properties of cortical neuron maturation. By comparing human and mouse cortical neuronal maturation at high temporal and cell resolution, we found a slower pattern of mitochondria development in human cortical neurons compared with the mouse, together with lower mitochondria metabolic activity, particularly oxidative phosphorylation. Stimulation of mitochondria metabolism in human neurons resulted in accelerated maturation, leading to excitable and complex cells weeks ahead of time. Our data identify mitochondria as important regulators of the pace of neuronal development underlying human-specific features of brain evolution.

Why big brains? A comparison of models for both primate and carnivore brain size evolution

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.

New Remains of Scandiavis mikkelseni Inform Avian Phylogenetic Relationships and Brain Evolution

Although an increasing number of studies are combining skeletal and neural morphology data in a phylogenetic context, most studies do not include extinct taxa due to the rarity of preserved endocasts. The early Eocene avifauna of the Fur Formation of Denmark presents an excellent opportunity for further study of extinct osteological and endocranial morphology as fossils are often exceptionally preserved in three dimensions. Here, we use X-ray computed tomography to present additional material of the previously described taxon Scandiavis mikkelseni and reassess its phylogenetic placement using a previously published dataset. The new specimen provides novel insights into the osteological morphology and brain anatomy of Scandiavis. The virtual endocast exhibits a morphology comparable to that of modern avian species. Endocranial evaluation shows that it was remarkably similar to that of certain extant Charadriiformes, yet also possessed a novel combination of traits. This may mean that traits previously proposed to be the result of shifts in ecology later in the evolutionary history of Charadriiformes may instead show a more complex distribution in stem Charadriiformes and/or Gruiformes depending on the interrelationships of these important clades. Evaluation of skeletal and endocranial character state changes within a previously published phylogeny confirms both S. mikkelseni and a putative extinct charadriiform, Nahmavis grandei, as charadriiform. Results bolster the likelihood that both taxa are critical fossils for divergence dating and highlight a biogeographic pattern similar to that of Gruiformes.

Cognitive and behavioral modernity in Homo erectus: skull globularity and hominin brain evolution

In this article we provide evidence that evolutionary pressures altered the cranial base and the mastoid region of the temporal bone more than the calvaria in the transition from H. erectus to H. sapiens. This process seems to have resulted in the evolution of more globular skull shape – but not as a result of expansion of the brain in the parietal regions but of reduction of the cranial base and the mastoid region relative to the parietals. Consequently, we argue that expansion of the parietals seems to be unrelated to brain evolution, but is more a by-product of reduction in other regions of the skull, reduction that may be related to dietary factors. Additionally, these findings suggest that cognitive and behavioural modernity may not necessarily be dependent on brain shape. Also, it cannot be attributed to the change in brain size because H. erectus and modern human cranial capacities overlap substantially. Consequently, we suggest H. erectus possessed the full suite of cognitive adaptations characteristic of modern humans without possessing a globular skull with flared parietals. Our results also support the theory that paedomorphic morphogenesis of the skull was important in the transition from H. erectus to H. sapiens and that such changes may be related to both dietary factors and social evolution.

Homo Paedens? Did Kids Invent the Human Species?

The evolution of development (“evo-devo”) has become a central concern in both evolu­tionary and developmental research, and human immaturity is no less a proper focus for evolutionary analysis than that of other species-if anything, it is more so. Two new books by David F. Bjorklund, a founder of evolutionary developmental psychology, summarize what we know now and propose that children invented our species. Due to the new phe­nomenon of partly heritable epigenetic modification of genes and the old one of the Bald­win Effect (by which plasticity leads to new selective forces on genes), this claim must be at least partly true. The inherent plasticity of children’s behavior, including play, accelerat­ed the evolution of humanity as instantiated in the human brain. Evolution cannot be understood without extensive reference to development, and nothing in childhood makes sense except in the light of evolution.

The HUSH complex controls brain architecture and protocadherin fidelity

Fine-tuning of neural connectivity is important for cerebral functions and brain evolution. Protocadherins provide barcodes for neuronal identity as well as synapse formation and expansion of protocadherin cluster genes has been linked to advanced cognitive functions. The tightly controlled stochastic and combinatorial expression of the different protocadherin isoforms in individual neurons provides the molecular basis for neuronal diversity, neuronal network complexity and function of the vertebrate brain. How protocadherins are epigenetically controlled has not yet been fully elucidated. Here we show that the HUSH (human silencing hub) complex containing H3K9me3 binding protein M-phase phosphoprotein 8 (MPP8) and Microrchidia CW-type zinc finger protein 2 (MORC2), critically controls the fidelity of protocadherin expression. MPP8 and MORC2A are highly expressed in the murine brain and exclusively found in neurons. Genetic inactivation of Mphosph8 (coding for MPP8) or Morc2a in the nervous system of mice leads to increased brain size, altered brain architecture, and behavioral changes. Mechanistically, MPP8 and MORC2A precisely and selectively suppress the repetitive-like protocadherin gene cluster on mouse chromosome 18 in a H3K9me3-dependent manner, thereby affecting synapse formation. Moreover, we demonstrate that individual MPHOSPH8- or MORC2-deficient neurons in human cerebral organoids express increased numbers of clustered protocadherin isoforms. Our data identify the HUSH complex, previously linked to silencing of repetitive transposable elements, as a key epigenetic regulator of protocadherin expression in the nervous system and thereby brain development and neuronal individuality in mice and humans.