Tinbergen's fourth question, ontogeny: sexual and individual differentiation

Abstract

Based on Tinbergen's view of the study of behavioural development we describe some recent advances and their importance in this field. We argue that the study of behavioural development should combine both proximate and ultimate approaches, and can help to understand how early subtle environmental factors shape consistent individual variation both between and within sexes. This is illustrated by reviewing the profound effects of incubation temperature on the development of brain and social behaviour in the leopard gecko, a species with temperature-dependent sex determination, and the effects of early exposure to steroid hormones on social behaviour in rodents and especially birds. Both are maternal effects: incubation temperature can be partly determined by the nest site where the mother deposited her eggs, while in both oviparous and viviparous vertebrates maternal hormones reach and influence the embryo. In the gecko, incubation temperature affects sexual and aggressive behaviour, growth, the hypothalamus-pituitary-gonadal axis, as well as the size, connectivity and metabolic capacity of certain brain areas. In this way not only is the gonad type determined, but so too is the morphological, physiological, neural, and behavioural phenotype established that explains much of within-sex variation. In rodents, maternal hormones affect similar aspects. In avian species, maternal hormones, deposited in the eggs, vary systematically between and within clutches and have both short-and long-lasting effects on competitive behaviour. Evidence suggests that mothers adaptively adjust hormone allocation to the environmental context. In addition, we discuss some effects of postnatal experience on behavioural development in geckos, mice and bird species. Our results also illustrate how the study of animal models other than rodents can help in understanding important developmental processes.

Unfolding personalities: The importance of studying ontogeny

“…However, different behaviors like aggression and sexual behavior activate a wide array of brain areas that largely overlap for both behaviors. Moreover, differences in behavior such as between femalelike males and more macho males in the gecko (that may be classified as differences in personality) are reflected in a wide array of overlapping brain areas (reviewed in Crews & Groothuis, 2005). This suggests that differences in personality may actually indicate differences in some fundamental aspect of the organization of behavior that affects more than one system, or, in the old terminology, more than one drive.…”

The development of behaviour: trends since Tinbergen (1963)

“…Gottlieb (1997) discusses many aspects of this debate, and we have recently republished some of the original papers (Bolhuis and Hogan, 1999). Crews and Groothuis (2005) address Tinbergen's discussion of ontogeny in some detail. Here, we will mention only two important issues.…”

“…It has become clear that the neural substrate for tutor song memory is likely to be found outside the 'song system', in the caudomedial nidopallium and/or the caudomedial mesopallium Terpstra et al, 2004). Another example of how these techniques are used to study developmental problems is the paper by Crews and Groothuis (2005). While molecular methods have been very useful in understanding many aspects of behavioural and neural development, it must be remembered that even a complete understanding of molecular mechanisms will not be sufficient for a complete understanding of behavioural development (Oppenheim, 2001).…”

“…Ten Cate and Bateson (1988) later reviewed the literature and concluded that sexual imprinting could play an important role in sexual selection and the evolution of conspicuous plumage (see also ten Cate and Vos, 1999). The paper by Crews and Groothuis (2005) gives other examples of how causal and functional thinking can complement each other in studies of development.…”

“…This is not, of course, the same as a change of behaviour during development;" (1963, p. 424). As Crews and Groothuis (2005) rightly point out, all of Tinbergen's "why" questions (i.e., causation, survival value, and evolution) can and should be asked of behavioural development. Nonetheless, in this paper, we will concentrate on Tinbergen's original concern with the causal mechanisms of development, and only mention functional and evolutionary aspects briefly in the concluding section.…”