Bioenergetics and evolutionary genetics: opportunities for new synthesis
Abstract
Bioenergetics, the study of energy flow through living systems, may be helpful in the study of evolutionary genetics, at least for those loci concerned with resource processing in metabolism. Energy flow through organisms is sensitive to resource supply and demand, to parameters of metabolic organization which are the kinetic constants and concentrations of the enzymes implementing metabolic pathways, and to state variables such as temperature, ionic strength, etc., on whose values metabolic parameters depend. Selection can therefore modify energy flow patterns, either by action on genetic variation in metabolic parameters, or by action on genetic variation in trait syndromes which "filter" environmental inputs into more or less regulated internal values of state variables. To understand the impact of such genetic variation on fitness-related aspects of organisms' phenotypes, it is essential to analyze correctly the effects on metabolic organization of single-locus changes in metabolic parameters. Expectations of the bioenergetic viewpoint are tested by reference to several case studies of allozyme polymorphism. In organisms ranging from E. coli to butterflies and mice, apparent visibility of genetic variation to selection, as indexed by effects on net fitness or fitness components, is scaled by interaction of the size of genotypic changes in metabolic parameters with the position of the locus in metabolism. At loci central to metabolism, large genotypic differences in kinetics or stability have clearly selectable effects, while small differences do not. In one critical case, a difference in kinetics between two alleles was invisible to selection while the locus was peripheral to major resource flow into the cell, but the same difference was clearly selected upon when allelic substitution elsewhere in the genome placed the locus in control of major resource flow into the cell. Evolutionary processes, thus, may often distinguish character states specific to individual loci, though for small differences and bioenergetically peripheral loci, selectable character states may be integrated at much higher levels of organization and may encompass many nearly equivalent genotypic combinations. Bioenergetics is an important, though not necessarily universal, tool in clarifying interaction of character states with selective pressures, and in making the study of adaptive mechanisms a more rigorous and integral part of evolutionary biology.
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