Modularity as a universal emergent property of biological traits.

An emergent property of an entity is one that results from the organization or interaction of its components. Here I argue that modularity (discreteness) is a universal emergent property of organismic traits that results from the universal bounded responsiveness, to inputs (e.g., genomic or environmental), of the phenotype at all levels of organization. While degree of modularity is variable and may be subject to change under selection, I argue that the consequences of modularity, such as the evolvability of modular traits (e.g., due to their somewhat independent expression and selection; and their potential for expression in new combinations) are not responsible for the existence of modularity itself. I discuss some other views of modularity in biology; and the related idea that increased complexity (e.g., increased numbers of kinds of modular traits) is a product of selection. I argue that emergent properties characterize innovative phenotypes at their origin. When emergent properties occur at more than one level of phenotypic organization, they sometimes lead to confusion due to confounding levels of organization with levels of selection, as has occurred in discussions of group selection in the evolution of sociality. Phenotypes, whose environmental sensitivity and (emergent) properties are emphasized here, seem likely to assume increasing importance as biology moves toward a better understanding of the genome as agent of both the transmission and the expression of traits.

Nutrition, the visceral immune system, and the evolutionary origins of pathogenic obesity.

The global obesity epidemic is the subject of an immense, diversely specialized research effort. An evolutionary analysis reveals connections among disparate findings, starting with two well-documented facts: Obesity-associated illnesses (e.g., type-2 diabetes and cardiovascular disease), are especially common in: (i) adults with abdominal obesity, especially enlargement of visceral adipose tissue (VAT), a tissue with important immune functions; and (ii) individuals with poor fetal nutrition whose nutritional input increases later in life. I hypothesize that selection favored the evolution of increased lifelong investment in VAT in individuals likely to suffer lifelong malnutrition because of its importance in fighting intraabdominal infections. Then, when increased nutrition violates the adaptive fetal prediction of lifelong nutritional deficit, preferential VAT investment could contribute to abdominal obesity and chronic inflammatory disease. VAT prioritization may help explain several patterns of nutrition-related disease: the paradoxical increase of chronic disease with increased food availability in recently urbanized and migrant populations; correlations between poor fetal nutrition, improved childhood (catch-up) growth, and adult metabolic syndrome; and survival differences between children with marasmus and kwashiorkor malnutrition. Fats and sugars can aggravate chronic inflammation via effects on intestinal bacteria regulating gut permeability to visceral pathogens. The extremes in a nutrition-sensitive trade-off between visceral (immune-function) vs. subcutaneous (body shape) adiposity may have been favored by selection in highly stratified premedicine societies. Altered adipose allocation in populations with long histories of social stratification and malnutrition may be the result of genetic accommodation of developmental responses to poor maternal/fetal conditions, increasing their vulnerability to inflammatory disease.

Darwin's forgotten idea: the social essence of sexual selection.

Darwinian sexual selection can now be seen in the broader context of social selection, or social competition for resources (under sexual selection, mates or fertilization success). The social-interaction aspects of sexually selected traits give them special evolutionary properties of interest for neurobiological studies of stimulus-response systems because they can account for highly complex systems with little information content other than stimulatory effectiveness per se. But these special properties have a long history of being forgotten when other factors dominate the analysis of male-female interactions, such as the mistaken belief that differential responsiveness to signals produced by competing rivals ("female choice") requires an esthetic sense; that species recognition explains all species-specific sexual signals; and, more recently, that successful signals must reflect good survival genes; or that male-female conflict involves female resistance rather than stimulus evaluation. A "conflict paradox" results when male-female conflict is seen as driven by natural selection, whose costs should often move the hypothesized "sexually antagonistic co-evolution" of sensory-response systems toward the powerful domain of sexually synergistic co-evolution under sexual selection. Special properties of sexual selection apply to other forms of social competition as well, showing the wisdom of Darwin's setting it apart from natural selection as an explanation of many otherwise puzzling and extreme traits.

Phenotypic accommodation: adaptive innovation due to developmental plasticity.

Phenotypic accommodation is adaptive adjustment, without genetic change, of variable aspects of the phenotype following a novel input during development. Phenotypic accommodation can facilitate the evolution of novel morphology by alleviating the negative effects of change, and by giving a head start to adaptive evolution in a new direction. Whether induced by a mutation or a novel environmental factor, innovative morphological form comes from ancestral developmental responses, not from the novel inducing factor itself. Phenotypic accommodation is the result of adaptive developmental responses, so the novel morphologies that result are not "random" variants, but to some degree reflect past functionality. Phenotypic accommodation is the first step in a process of Darwinian adaptive evolution, or evolution by natural selection, where fitness differences among genetically variable developmental variants cause phenotype-frequency change due to gene-frequency change.

The maintenance of sex as a developmental trap due to sexual selection.

The writings of George Williams challenged biologists to think critically about levels of selection, social behavior, and the paradox of sex, whose maintenance by recombination alone has not been convincingly demonstrated in theory or in fact. A solution is suggested by observations of the dependence of females on interaction with males, as a result of sexual selection. This, along with recombination in changing environments and DNA repair during meiosis, may contribute to a pluralistic explanation for the maintenance of sex.

Developmental plasticity and the origin of species differences.

Speciation is the origin of reproductive isolation and divergence between populations, according to the "biological species concept" of Mayr. Studies of reproductive isolation have dominated research on speciation, leaving the origin of species differences relatively poorly understood. Here, I argue that the origin of species differences, and of novel phenotypes in general, involves the reorganization of ancestral phenotypes (developmental recombination) followed by the genetic accommodation of change. Because selection acts on phenotypes, not directly on genotypes or genes, novel traits can originate by environmental induction as well as mutation, then undergo selection and genetic accommodation fueled by standing genetic variation or by subsequent mutation and genetic recombination. Insofar as phenotypic novelties arise from adaptive developmental plasticity, they are not "random" variants, because their initial form reflects adaptive responses with an evolutionary history, even though they are initiated by mutations or novel environmental factors that are random with respect to (future) adaptation. Change in trait frequency involves genetic accommodation of the threshold or liability for expression of a novel trait, a process that follows rather than directs phenotypic change. Contrary to common belief, environmentally initiated novelties may have greater evolutionary potential than mutationally induced ones. Thus, genes are probably more often followers than leaders in evolutionary change. Species differences can originate before reproductive isolation and contribute to the process of speciation itself. Therefore, the genetics of speciation can profit from studies of changes in gene expression as well as changes in gene frequency and genetic isolation.

Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis.

Previous studies of the division of labor in colonies of eusocial Hymenoptera (wasps and bees) have led to two hypotheses regarding the evolution of juvenile hormone (JH) involvement. The novel- or single-function hypothesis proposes that the role of JH has changed from an exclusively reproductive function in primitively eusocial species (those lacking morphologically distinct queen and worker castes), to an exclusively behavioral function in highly eusocial societies (those containing morphologically distinct castes). In contrast, the split-function hypothesis proposes that JH originally functioned in the regulation of both reproduction and behavior in ancestral solitary species. Then, when reproductive and brood-care tasks came to be divided between queens and workers, the effects of JH were divided as well, with JH involved in regulation of reproductive maturation of egg-laying queens, and behavioral maturation, manifested as age-correlated changes in worker tasks, of workers. We report experiments designed to test these hypotheses. After documenting age-correlated changes in worker behavior (age polyethism) in the neotropical primitively eusocial wasp Polistes canadensis, we demonstrate that experimental application of the JH analog methoprene accelerates the onset of guarding behavior, an age-correlated task, and increases the number of foraging females; and we demonstrate that JH titers correlate with both ovarian development of queens and task differentiation in workers, as predicted by the split-function hypothesis. These findings support a view of social insect evolution that sees the contrasting worker and queen phenotypes as derived via decoupling of reproductive and brood-care components of the ancestral solitary reproductive physiology.