Adaptive significance of natural variations in maternal care in rats: a translational perspective

Abstract

A wealth of data from the last fifty years documents the potency of early life experiences including maternal care on developing offspring. A majority of this research has focused on the developing stress axis and stress-sensitive behaviors in hopes of identifying factors impacting resilience and risk-sensitivity. The power of early life experience to shape later development is profound and has the potential to increase fitness of individuals for their environments. Current findings in a rat maternal care paradigm highlight the complex and dynamic relation between early experiences and a variety of outcomes. In this review we propose adaptive hypotheses for alternate maternal strategies and resulting offspring phenotypes, and suggest means of distinguishing between these hypotheses. We also provide evidence underscoring the critical role of context in interpreting the adaptive significance of early experiences. If our goal is to identify risk-factors relevant to humans, we must better explore the role of the social and physical environment in our basic animal models.

Figure 1

Time-scales of adaptation and sample genetic mechanisms. Organisms adapt to their environments in both temporary and long-term ways; adaptation involves processes including regulation across these time-scales with different regulatory mechanisms allowing for distinct temporal patterns of regulation.

Figure 2

Schema of maternal strategy, offspring fitness, and expected phenotype abundance. If variation in maternal care is not adaptive, one would offspring fitness to be unrelated to maternal investment (panel A). To the extent that maternal behavior is adaptive, high maternal investment in offspring should be associated with an increase in offspring fitness to offset time and energy costs (panel B, C upper right); higher investment associated with lower offspring fitness (lower right) does not represent an optimal reproductive strategy. Low maternal investment under conditions of relative environmental adversity may be advantageous despite the potential for low fitness of the offspring (panel B, lower left) because the mother may increase her odds of survival to future reproduction. In contrast, if offspring of females providing low levels of maternal care are routinely of high fitness for their local environment, this may represent tuning (panel C, upper left).