Review. Do hormonal control systems produce evolutionary inertia?

Abstract

Hormonal control systems are complex in design and well integrated. Concern has been raised that these systems might act as evolutionary constraints when animals are subject to anthropogenic environmental change. Three systems are examined in vertebrates, especially birds, that are important for assessing this possibility: (i) the hypothalamic-pituitary-gonadal (HPG) axis, (ii) the activational effects of sex steroids on mating effort behaviour, and (iii) sexual differentiation. Consideration of how these systems actually work that takes adequate account of the brain's role and mechanisms suggests that the first two are unlikely to be impediments to evolution. The neural and molecular networks that regulate the HPG provide both phenotypic and evolutionary flexibility, and rapid evolutionary responses to selection have been documented in several species. The neuroendocrine and molecular cascades for behaviour provide many avenues for evolutionary change without requiring a change in peripheral hormone levels. Sexual differentiation has some potential to be a source of evolutionary inertia in birds and could contribute to the lack of diversity in certain reproductive (including life history) traits. It is unclear, however, whether that lack of diversity would impede adaptation to rapid environmental change given the role of behavioural flexibility in avian reproduction.

Figure 1

Endocrine axes, including the HPG axis. See text for description. (Adapted from Norris (1996). Copyright © Academic Press (Elsevier).)

Figure 2

Mechanisms of action of steroid hormones on neurons. See text for description. (Reproduced with permission from Weeks & Levine (1995). Copyright © 2000 Elsevier Science).

Figure 3

Gene expression during gonadal sex differentiation in the chicken embryo. Circles indicate the onset of gene expression. (Reproduced with permission from Smith & Sinclair (2004). Copyright © 2004 Wiley Periodicals, Inc.)

Figure 4

Organization by embryonic gonadal hormones of adult sex differences in the brain and behaviour of Japanese quail. See text for description.

Figure 5

Proposed mechanisms of sexual differentiation in the preoptic region of the male rat brain. The initiating signal is oestradiol (E₂) derived from testosterone (T) by brain aromatization. COX-2, enzyme involved in the synthesis of PGE₂ (prostaglandin-E₂, which is both necessary and sufficient for masculinization of mating by E₂); AA, arachidonic acid; EP1-3, prostaglandin receptor subtypes 1–3; A/K, AMPA/Kainate glutamate receptor. (Reproduced with permission from McCarthy et al. (2003). Copyright © 2003 New York Academy of Sciences.)