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].