Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'

Abstract

Twenty years ago, Albert Bennett published a paper in the influential book New directions in ecological physiology arguing that individual variation was an 'underutilized resource'. In this paper, I review our state of knowledge of the magnitude, mechanisms and functional significance of phenotypic variation, plasticity and flexibility in endocrine systems, and argue for a renewed focus on inter-individual variability. This will provide challenges to conventional wisdom in endocrinology itself, e.g. re-evaluation of relatively simple, but unresolved questions such as structure-function relationships among hormones, binding globulins and receptors, and the functional significance of absolute versus relative hormone titres. However, there are also abundant opportunities for endocrinologists to contribute solid mechanistic understanding to key questions in evolutionary biology, e.g. how endocrine regulation is involved in evolution of complex suites of traits, or how hormone pleiotropy regulates trade-offs among life-history traits. This will require endocrinologists to embrace the raw material of adaptation (heritable, individual variation and phenotypic plasticity) and to take advantage of conceptual approaches widely used in evolutionary biology (selection studies, reaction norms, concepts of evolutionary design) as well as a more explicit focus on the endocrine basis of life-history traits that are of primary interest to evolutionary biologists (cf. behavioural endocrinology).

Figure 1

Outlier or natural extreme phenotype? Most researchers would exclude the individual with the hematocrit value less than 35% in (a) as a statistical ‘outlier’; however, this individual laid two clutches of six eggs (b) with the largest mean egg size.

Figure 2

Comparison of results of (a) a cross-sectional versus (b) repeated measures analysis given marked inter-individual variation in a physiological trait; data compare hematocrit for non-breeding and egg-laying birds.

Figure 3

Examples of ‘physiological reaction norms’ in relation to (a) external and (b) internal environment. (a) Variation in plasma yolk precursor levels in egg-laying females maintained at three different ambient temperatures and (b) variation in oestrogen-induced (E2) anaemia (decrease in hematocrit) in relation to manipulated hormonal ‘environment’ (see text for more details).

Figure 4

‘Adapative’ hypotheses which propose effects of variation in mean hormone levels on phenotypic traits fail to explain why much larger inter-individual variation does not generate even greater phenotypic variation; this is illustrated with data on laying sequence-specific variation in yolk androgen levels (based on data in fig. 1d, Groothuis et al. 2006; see text for more details).