Understanding well-being in the evolutionary context of brain development

Much of the work on well-being and positive emotions has tended to focus on the adult, partly because this is when problems are manifest and well-being often becomes an issue by its absence. However, it is pertinent to ask if early life events might engender certain predispositions that have consequences for adult well-being. The human brain undergoes much of its growth and development postnatally until the age of seven and continues to extend its synaptic connections well into the second decade. Indeed, the prefrontal association cortex, areas of the brain concerned with forward planning and regulatory control of emotional behaviour, continue to develop until the age of 20. In this article, I consider the significance of this extended postnatal developmental period for brain maturation and how brain evolution has encompassed certain biological changes and predispositions that, with our modern lifestyle, represent risk factors for well-being. An awareness of these sensitive phases in brain development is important in understanding how we might facilitate secure relationships and high self-esteem in our children. This will provide the firm foundations on which to develop meaningful lifestyles and relationships that are crucial to well-being.     

The Expensive Brain: A framework for explaining evolutionary changes in brain size

To explain variation in relative brain size among homoiothermic vertebrates, we propose the Expensive Brain hypothesis as a unifying explanatory framework. It claims that the costs of a relatively large brain must be met by any combination of increased total energy turnover or reduced energy allocation to another expensive function such as digestion, locomotion, or production (growth and reproduction). Focusing on the energetic costs of brain enlargement, a comparative analysis of the largest mammalian sample assembled to date shows that an increase in brain size leads to larger neonates among all mammals and a longer period of immaturity among monotokous precocial species, but not among the polytokous altricial ones, who instead reduce their litter size. Relatively large brained mammals, altricial and precocial, also show reduced annual fertility rates as compared to their smaller brained relatives, but allomaternal energy inputs allow some cooperatively breeding altricial carnivores to produce even more offspring in a shorter time despite having a relatively large brain. Thus, the Expensive Brain framework explains why brain size is linked to life history pace in some, but not all mammalian lineages. This framework encompasses other hypotheses of energetic constraints on brain size variation and is also compatible with the Brain Malnutrition Risk hypothesis, but the absence of a mammal-wide correlation between brain size and immature period argues against the Needing-to-Learn explanation for slower development among large brained mammals.     

Control of behavioral development in the context of reintroduction programs for birds

Only over the last few decades has there been a concerted effort to develop and refine release methods for threatened species. With the goal of achieving self-sustaining wild populations, three main techniques have been employed: parent-rearing, cross-fostering, and isolation-rearing. Although there are many considerations in developing or selecting the most efficient method for any given species, the behavioral aspects of preparing birds for release are important. The concept of different life history strategies may also help in designing a preparation and release methodology. The degree of interspecific and intraspecific sociality also is important in the development of effective behavioral preparation of individuals for release. © 1994 Wiley-Liss, Inc.     

Brain development and predation: plastic responses depend on evolutionary history

Although the brain is known to be a very plastic organ, the effects of common ecological interactions like predation or competition on brain development have remained largely unexplored. We reared nine-spined sticklebacks (Pungitius pungitius) from two coastal marine (predation-adapted) and two isolated pond (competition-adapted) populations in a factorial experiment, manipulating perceived predatory risk and food supply to see (i) if the treatments affected brain development and (ii) if there was population differentiation in the response to treatments. We detected differences in plasticity of the bulbus olfactorius (chemosensory centre) between habitats: marine fish were not plastic, whereas pond fish had larger bulbi olfactorii in the presence of perceived predation. Marine fish had larger bulbus olfactorius overall. Irrespective of population origin, the hypothalamus was smaller in the presence of perceived predatory risk. Our results demonstrate that perceived predation risk can influence brain development, and that the effect of an environmental factor on brain development may depend on the evolutionary history of a given population in respect to this environmental factor.     

Role of CpG context and content in evolutionary signatures of brain DNA methylation

DNA methylation is essential in brain function and behavior; therefore, understanding the role of DNA methylation in brain-based disorders begins with the study of DNA methylation profiles in normal brain. Determining the patterns and scale of methylation conservation and alteration in an evolutionary context enables the design of focused but effective methylation studies of disease states. We applied an enzymatic-based approach, Methylation Mapping Analysis by Paired-end Sequencing (Methyl-MAPS), which utilizes second-generation sequencing technology to provide an unbiased representation of genome-wide DNA methylation profiles of human and mouse brains. In this large-scale study, we assayed CpG methylation in cerebral cortex of neurologically and psychiatrically normal human postmortem specimens, as well as mouse forebrain specimens. Cross-species human-mouse DNA methylation conservation analysis shows that DNA methylation is not correlated with sequence conservation. Instead, greater DNA methylation conservation is correlated with increasing CpG density. In addition to CpG density, these data show that genomic context is a critical factor in DNA methylation conservation and alteration signatures throughout mammalian brain evolution. We identify key genomic features that can be targeted for identification of epigenetic loci that may be developmentally and evolutionarily conserved and wherein aberrations in DNA methylation patterns can confer risk for disease.     

Role of CpG context and content in evolutionary signatures of brain DNA methylation

DNA methylation is essential in brain function and behavior; therefore, understanding the role of DNA methylation in brain-based disorders begins with the study of DNA methylation profiles in normal brain. Determining the patterns and scale of methylation conservation and alteration in an evolutionary context enables the design of focused but effective methylation studies of disease states. We applied an enzymatic-based approach, Methylation Mapping Analysis by Paired-end Sequencing (Methyl-MAPS), which utilizes second-generation sequencing technology to provide an unbiased representation of genome-wide DNA methylation profiles of human and mouse brains. In this large-scale study, we assayed CpG methylation in cerebral cortex of neurologically and psychiatrically normal human postmortem specimens, as well as mouse forebrain specimens. Cross-species human-mouse DNA methylation conservation analysis shows that DNA methylation is not correlated with sequence conservation. Instead, greater DNA methylation conservation is correlated with increasing CpG density. In addition to CpG density, these data show that genomic context is a critical factor in DNA methylation conservation and alteration signatures throughout mammalian brain evolution. We identify key genomic features that can be targeted for identification of epigenetic loci that may be developmentally and evolutionarily conserved and wherein aberrations in DNA methylation patterns can confer risk for disease.     

Adaptive aging in the context of evolutionary theory

Compelling evidence for an adaptive origin of aging has clashed with traditional evolutionary theory based on exclusively individual selection. The consensus view has been to try to understand aging in the context of a narrow, restrictive evolutionary paradigm, called the Modern Synthesis, or neo-Darwinism. But neo-Darwinism has shown itself to be inadequate in other ways, failing to account for stable ecosystems, for the evolution of sex and the maintenance of diversity and the architecture of the genome, which appears to be optimized for evolvability. Thus aging is not the only reason to consider overhauling the standard theoretical framework. Selection for stable ecosystems is rapid and efficient, and so it is the easiest modification of the neo-Darwinian paradigm to understand and to model. Aging may be understood in this context. More profound and more mysterious are the ways in which the process of evolution itself has been transformed in a bootstrapping process of selection for evolvability. Evolving organisms have learned to channel their variation in ways that are likely to enhance their long-term prospects. This is an expanded notion of fitness. Only in this context can the full spectrum of sophisticated adaptations be understood, including aging, sex, diversity, ecological interdependence, and the structure of the genome.     

Thoughts on clonal integration: Facing the evolutionary context

Summary In this essay, I have pointed out that the appropriate evolutionary context for plant clonality dictates a focus on the impact of the derived trait of potential independence of subunits on the evolutionarily primitive trait of obligate interdependence of plant subunits, i.e. the advantages of independence. This fact prescribes a major shift in approach from previous lines of investigation which have assumed that clonal plants should fall apart and sought to determine the advantages of interdependence. The delineated reorientation calls for a significant change in the investigation of the ecology of clonality in higher plants, emphasizing factors that select for physical and physiological disintegration of the genet and de-emphasizing the need to derive ecological explanations for properties a plant will possess entirely by reason of its phylogenetic and developmental heritage. I suggest that (1) patterns of ramet independence may result from selective pressures on the cost of interconnections (2) programmed ramet independendence may be a response to the selective pressure of a high possibility of traumatic breakage and (3) programmed ramet independence may allow escape of the genet from mortality due to pathogen infestation.     

Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism

We describe a new hypothesis for the development of autism, that it is driven by imbalances in brain development involving enhanced effects of paternally expressed imprinted genes, deficits of effects from maternally expressed genes, or both. This hypothesis is supported by: (1) the strong genomic-imprinting component to the genetic and developmental mechanisms of autism, Angelman syndrome, Rett syndrome and Turner syndrome; (2) the core behavioural features of autism, such as self-focused behaviour, altered social interactions and language, and enhanced spatial and mechanistic cognition and abilities, and (3) the degree to which relevant brain functions and structures are altered in autism and related disorders. The imprinted brain theory of autism has important implications for understanding the genetic, epigenetic, neurological and cognitive bases of autism, as ultimately due to imbalances in the outcomes of intragenomic conflict between effects of maternally vs. paternally expressed genes.     

Hemolymph amino acid variations following behavioral and genetic changes in individual Drosophila larvae

This study investigated the effect of different sampling environments on hemolymph amino acid content of individual Drosophila melanogaster larvae. Hemolymph was collected from individual third instar larvae under cold-anesthetized, awake, and stress conditions. Qualitative and quantitative hemolymph amino acid analyses were performed via capillary electrophoresis with laser-induced fluorescence detection. The hemolymph amino acid concentrations, particularly arginine, glutamate, and taurine, changed significantly depending on the prior-to-sample-collection environments. Hemolymph amino acid analyses of six different Drosophila genotypes including two control genotypes and four mutant alleles were also carried out. Two mutant genotypes with over and under expression of a putative cystine-glutamate exchanger subunit were significantly different from each other with respect to their hemolymph glutamate, glycine, lysine, and taurine levels. Hemolymph amino acid analyses of stressed larvae of two control and two mutant genotypes indicated that behavior-related hemolymph chemical changes are also genotype dependent.     

How development changes evolution: conceptual and historical issues in evolutionary developmental biology

Evolutionary developmental biology (Evo-Devo) is a new and rapidly developing field of biology which focuses on questions in the intersection of evolution and development and has been seen by many as a potential synthesis of these two fields. This synthesis is the topic of the books reviewed here. Integrating Evolution and Development (edited by Roger Sansom and Robert Brandon), is a collection of papers on conceptual issues in Evo-Devo, while From Embryology to Evo-Devo (edited by Manfred Laubichler and Jane Maienschein) is a history of the problem of the relations between ontogeny and phylogeny.

Molecular and evolutionary computation: the tug of war between context freedom and context sensitivity

Proteins and nucleic acids constitute a vast potential reservoir of pattern recognizers that operate on the basis of shape complementarity. It is possible to construct models of computing in which these shape-based interactions contribute directly to recognition of signal patterns at the device (or cell) level. The input-output transform is molded by variation-selection evolution. Such models provide clues as to the organizational features that enable biomolecular matter to acquire nonevolutionary modes of problem solving through the evolutionary process. The requisite organizations are characterized by a high dimensionality that allows them to simultaneously exhibit aspects of context-sensitivity and context-independence.     

The interrelation between individual behavioral characteristics and the indices of brain energy metabolism in rats]

In rats with active type of behaviour in "open field" and "forced swimming" tests in response to weak stress (handling) both the rate of local blood flow (RLBF) and free oxygen tension level (pO2) in the brain are increased, and in rats with passive type of behaviour RLBF is increased, but the pO2 level is decreased. The character of pO2 level changes in the brain under stress is significantly (r = -0.74, p less than 0.001) connected with the level of depressiveness (time of passive swimming) and is nonsignificantly connected with the level of the motor activity. Indices of the active type of behaviour (the number of crossed squares, rearings, comings out to the center of the field and the time of extinction of the motor activity) positively correlate with succinate dehydrogenase (SDG) activity and negatively with NADH-dehydrogenase (NADH-DG) activity and the index of the passive type of behaviour (time of passive swimming) positively correlates with NADH-DG activity and negatively--with SDG activity.     

Increased brain signal variability accompanies lower behavioral variability in development

As the brain matures, its responses become optimized. Behavioral measures show this through improved accuracy and decreased trial-to-trial variability. The question remains whether the supporting brain dynamics show a similar decrease in variability. We examined the relation between variability in single trial evoked electrical activity of the brain (measured with EEG) and performance of a face memory task in children (8–15 y) and young adults (20–33 y). Behaviorally, children showed slower, more variable response times (RT), and less accurate recognition than adults. However, brain signal variability increased with age, and showed strong negative correlations with intrasubject RT variability and positive correlations with accuracy. Thus, maturation appears to lead to a brain with greater functional variability, which is indicative of enhanced neural complexity. This variability may reflect a broader repertoire of metastable brain states and more fluid transitions among them that enable optimum responses. Our results suggest that the moment-to-moment variability in brain activity may be a critical index of the cognitive capacity of the brain.     

The integrated development of network complexity modulates the diverse evolutionary mutation rates of individual proteins

The rate of evolution-related mutation varies widely among proteins while the unity of the organism implies an integrated evolution of its protein network. Focusing on the yeast interactome, we monitored the structural impact of amino acid substitution on yeast proteins with reported structure. The impact of mutation in creating or deleting structural markers for interactivity varies across proteins and modulates the evolutionary rates, yielding a unified kinetic law of accumulation of connectivities consistent with an integrated evolution of the interactome.     

New model systems for studying the evolutionary biology of aging: Crustacea

Progress in any area of biology has generally required work on a variety of organisms. This is true because particular species often have characteristics that make them especially useful for addressing specific questions. Recent progress in studying the evolutionary biology of senescence has been made through the use of new species, such asCaenorhabditis elegans andDrosophila melanogaster, because of the ease of working with them in the laboratory and because investigators have used theories for the evolution of aging as a basis for discovering the underlying mechanisms.I describe ways of finding new model systems for studying the evolutionary mechanisms of aging by combining the predictions of theory with existing information about the natural history of organisms that are well-suited to laboratory studies. Properties that make organisms favorable for laboratory studies include having a short generation time, high fecundity, small body size, and being easily cultured in a laboratory environment. It is also desirable to begin with natural populations that differ in their rate of aging. I present three scenarios and four groups of organisms which fulfill these requirements. The first two scenarios apply to well-documented differences in age/size specific predation among populations of guppies and microcrustacea. The third is differences among populations of fairy shrimp (anostraca) in habitat permanence. In all cases, there is an environmentla factor that is likely to select for changes in the life history, including aging, plus a target organism which is well-suited for laboratory studies of aging.