A multiplicity of factors and forces, including genetic, environmental and stochastic ones, influence how organisms grow and develop. This is so with respect to reproductively significant traits, a primary focus of this report, such as maturational tempo and pubertal timing [1]. Life-history theory is a powerful evolutionary framework [2, 3] for understanding a second focus of this essay: adaptive development plasticity, particularly with regard to growth- and metabolic-related strategies for transitioning from one life-history phase to the next [4–6].

When it comes to the environmental regulation of life history, the time of maximal developmental plasticity appears to be during the prenatal and early postnatal periods [6]. Indeed, the infancy-to-childhood transition (ICT) is often a time of heightened nutritional stress and mortality in humans, thereby representing a bottleneck for evolutionary forces. In social mammals, including apes, as well as in traditional human societies, the ICT is the time of weaning from breastfeeding, a third important focus here, demarcating the transition from maternal provision, protection and support to greater independence. Weaning from lactation is itself responsive to sex, stress and other environmental cues [7] that are presumed to inform the developing organism about risks and opportunities in its current and future environment. As such, the timing of the ICT has been hypothesized to reflect the adaptive adjustment of a species or an individual's size to the prevailing and anticipated environment, as the ICT is a major determinant of final adult height [5].

This view, that weaning is regulated by contextual conditions and serves to regulate life history in the service of fitness goals, led us to test experimentally in rats the proposition that the age of weaning, our index of ICT, provides cues for growth, maturation, developmental tempo and litter size, thereby affecting these outcomes. We also evaluate the proposition that such effects of weaning age are enhanced across generations in rats.

To evaluate effects of weaning age on life-history traits in rats, as well as on their offspring's development, we repeatedly measured length and BMI, as well as physiological development and sexual maturation in pups weaned early (d16), normally (d21) or late (d26). Due to concerns that the effects of maternal care on behavior could be reversed by cross-fostering [8, 9], steps were taken to eliminate this possibility: weaning was accomplished through cross-fostering by non-lactating mothers, and separation was carried out on d30 for all. By the nature of that design, timing of weaning is confounded by time spent with a foster mother. Upon removal of lactating mothers, food was supplied ad lib as both chow and powder to ascertain its reach by all pups.

The findings presented here on rats lend support to the proposition that the duration of infancy, as indexed by weaning age, predicts and perhaps programs growth, body composition, and the tempo of physiological development and maturation, as well as litter size and parity, and, thereby, reproductive strategy.

Two important environmental cues for development of the young animal (and humans) are 1) the care-giving behaviors of their parents, which can be used as a predictive indicator of the security of their environment, and 2) provision of nutrition during the immediate postnatal period, which may predict nutritional availability during future life. The resultant patterns will be transmitted trans-generationally [16, 17]. In view of prior evidence that weaning in rats has unique and critical effects on adult behavior [18], the data presented here indicate that weaning age influenced development in a manner consistent with an insecure, fast, life-history strategy (15), including accelerated growth, development and maturation, long/thin stature and, in subsequent generations, large litter size. In contrast, prolonged lactation influenced development in a manner consistent with a secure, slow, life-history strategy, including slower growth, development and maturation, short/overweight stature, and, in subsequent generations, small litter size. Yet, under natural conditions, early weaning might well be associated with more robust nutritional conditions that lead to more rapid pup growth and an earlier attainment of an appropriate size for independence. Similarly, in humans living in subsistence ecological contexts, early weaning is associated with better nutritional conditions.

The growth-promoting effect in rats of short infancy is much in line with human observations on the growth impact of early ICT [4, 5]. We have proposed that adult size is determined to an important extent during transition from infancy to childhood. This transition is marked by a growth spurt. A delayed transition has a lifelong impact on stature and is responsible for 44% of children with short stature in developed countries, and many more in developing countries. This conformed with the theory of an evolutionary adaptive strategy of plasticity in the timing of transition from infancy into childhood in order to match the prevailing energy supply: humans evolved to withstand energy crises by decreasing their body size, and evolutionary short-term adaptations to energy crises trigger a predictive adaptive response that modify the transition into childhood, culminating in short stature [1, 6].

The apparent tempo-accelerating effect in infantile developmental milestones of parental short lactation in the rat indicates a developmental signal transmitted across generations and seemingly aimed to prepare the young animal for independence for provision and protection upon weaning. This raises the interesting question of exactly how short lactation accelerates development, as we have provided evidence that it does, not of the underlying neurobiological mechanisms involved. Future work will need to illuminate such processes. In any event, it is of interest that early sexual maturation and large litters in animals are in line with an accelerated life history tempo brought about by shortening of the infancy stage. In swine, sows' parity number and litter size increase as lactation is prolonged from 8 to 13 to 18 to 21 days, but decrease if lactation is further prolonged to 22 to 25 days [19], in agreement with the rat findings.

Asymmetries in the costs and benefits of parental investment for mothers and fathers result in family conflict over their offspring's growth [20]. In species where females provide most resources before and after birth, the resolution of this conflict may be influenced by genes expressed in mothers and by maternally and paternally inherited genes expressed in offspring [21]. Here we show that the weaning-related trait is transmitted from the paternal side; offspring of fathers but not of mothers who weaned early were longer, thinner and had earlier sexual maturation. Previous work in mice showed that differences in litter size are determined by paternal genotype, whereas differences in provisioning are under maternal control, suggesting that there is antagonistic coadaptation of maternal and paternal effects on distinct life-history traits [21]. These results are consistent with a negative correlation that we discerned between the age of the infancy-childhood growth transition and fathers' height but not mothers' heights [6], leading us to conclude that the trans-generational transmission of transition age appears paternally derived.

The fact that the glucose intolerance and insulin resistance were related to delayed weaning is considered a response to being overweight. The thrifty phenotype theory suggests that intrauterine wasting and early infantile growth acceleration are associated with later acquisition of obesity and insulin resistance [22]. Indeed, on d10 offspring of late weaned animals, which are to become overweight as adults, had diminished adipose tissue, suggesting that the adult phenotype may be influenced by infantile expansion of the adipose tissue [23].

Considered together, the animal results reported support a conditional-adaptational view of individual differences in the infantile stage: developmental tempo and pubertal maturation are accelerated adaptively in response to shortening of infancy to allow for juvenile independence upon early weaning (development) and earlier reproduction (sexual maturation) [24].

In the discussion of nature and nurture, our results lend support to a major impact of a conditional adaptation within a single generation, and provide insight into the role of plasticity over one-to-three generations in reproductively important traits such as size, developmental and maturational tempo. The notion that developmental tempo is regulated by weaning age to produce such contrasting phenotypes, and that fathers transmit the trait, has significant implications for evolutionary biology as well as to child growth and maturation in a changing society.