Hormone-mediated suites as adaptations and evolutionary constraints

Abstract

Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.

Figure 1

Schematic of the effect of genetic covariance on selection response. The magnitudes of the elements of G were chosen arbitrarily. The diagonal elements of G represent additive genetic variance for each trait, z₁ and z₂, and the off-diagonal element represents a positive genetic covariance between the two traits. Directional selection is represented by the vector β, and the magnitude of the elements is the median from studies of natural populations (Kingsolver et al. 2001). Response to selection acting in the same direction on both traits, that is, on the major axis of the correlation (a) is facilitated by genetic covariance, and the selection response ($\mathrm{\Delta }\overline{\mathit{z}}$) is positive for both traits. Response to selection acting in opposite directions, that is, on the minor axis (b) is constrained, as shown by the small values in $\mathrm{\Delta }\overline{\mathit{z}}$.

Figure 2

Hypothetical example of the effect of correlational selection on hormone-mediated trait suites. The plots on the left are individual fitness surfaces, with two traits, z₁ and z₂, on the horizontal axes and relative fitness, w, on the vertical axis (Brodie et al. 1995). In (a), the two traits are regulated by a common hormone, as represented by the circle on the right. As in figure 1, each has a genetic variance G=0.5, and the genetic covariance is G₁₂=0.75. The fitness surface shows natural selection on the two traits. Both traits are under moderate directional selection, β=0.16, and stabilizing selection, γ=0.1 (medians from Kingsolver et al. 2001), and are affected by relatively strong correlational selection, γ₁₂=0.3. Using the equation ΔG=G(γ−ββ^T), this selective regime is predicted to maintain the correlation between the traits, and hence, their common hormonal basis. In (b), the direction of selection on z₂ is reversed (β=−0.16), and there is no correlational selection. Within one generation, a decrease in the genetic correlation is predicted. Over several generations, z₂ may become disassociated from hormonal regulation. In (c), negative correlational selection (γ₁₂=−0.3) also occurs, accelerating the dissociation of z₂.