Abstract

Studies across multiple organisms reveal considerable phenotypic variation in reproductive tactics. In some species, this variation is associated with maternal effects in which variation in maternal investment results in stable individual differences in reproductive function. Recent studies with the rat suggest that maternal effects can alter the function of neuroendocrine systems associated with female sexual behaviour as well as maternal behaviour. These maternal effects appear to be mediated by epigenetic modifications at the promoter for oestrogen receptor alpha (ERα) and subsequent effects on gene expression. The tissue‐specific nature of such effects may underlie the co‐ordinated variation in multiple forms of reproductive function, resulting in distinct reproductive strategies.

In the hunt for more reliable genotype–phenotype relations, few examples would seem as potentially rewarding as that describing the Y chromosome effect on gonadal differentiation in mammals. Thus, genetic sex (XX or XY) determines gonadal phenotype, from which derives the process of sexual differentiation into the male or female phenotype, or gender (1–4). However, a preoccupation with sexual differentiation neglects the intriguing issue of individual differences in the expression of traits directly associated with reproduction across members of the same sex (5, 6). We might assume that more complex functions, such as behaviour, admit more readily to variation between individuals of the same species (although variations in form across members of the same species have been underestimated; e.g. 7). Indeed, the pathways that lead from gonadal differentiation to differentiation of the HPG axis and behaviour are subject to considerable regulation, and thus variation in sexual differentiation within members of the same gender should not be surprising.

It is commonly thought that the capacity for phenotypic plasticity evolved to permit diversity in genotype–phenotype relations in response to variations in the level of environmental demands (7, 8). Such phenotypic diversity is likely to reflect complex gene–environment interactions involving protein–DNA interactions at sites (e.g. promoters, enhancers and suppressors) that regulate gene expression. It is interesting that, across species, increasing complexity is associated more with the size of the non‐coding region of the genome than with the number of genes. We presume that this difference reflects the increased complexity of the regulatory regions of the DNA that, in turn, confers enhanced capacity for tissue‐specific regulation of gene expression in multi‐organ animals. In addition, the increased size of the regulatory region of the genome should also correspond to an increased capacity for environmental regulation of gene expression – a process whereby an increasing range of phenotypes might emerge from a common genotype: an increased capacity for phenotypic plasticity.