The concept of adaptation assumes that organisms optimize their evolutionary fitness by improving their ability to survive and breed in a given environment. Adaptive variation in body size is predicted to emerge through cumulative
J.C.K. Wells (*)
Childhood Nutrition Research Centre, UCL Institute of Child Health,
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK © Springer Science+Business Media New York 2017
G. Jasienska et al. (eds.), The Arc of Life, DOI 10.1007/978-1-4939-4038-7_3
trade-offs between the life history functions of survival, growth, and reproduction, as shaped by diverse ecological factors (Harvey et al. 1987; Hill 1993). In humans, variability in adult size has been associated with factors such as the thermal environment, energy supply, and mortality risk (Katzmarzyk and Leonard 1998; Walker et al. 2006). A portion of this variability appears to have occurred as a result of natural selection acting directly on genetic variability, since over 200 genes have now been associated with adult height in humans (Lango Allen et al. 2010), and the trait has high heritability (Silventoinen et al. 2003; though see Wells and Stock 2011).
In addition to genotype, phenotypic plasticity represents an alternative means whereby organisms can respond to ecological stresses (West-Eberhard 2003). It might appear intuitive that phenotypic plasticity should favor adaptation to ecological conditions—however, not all plasticity results in greater htness (Via et al. 1995; Ellison and Jasienska 2007). For human body size, some of the variability in adult phenotype derives from growth variability early in the life course. Growth becomes increasingly canalized from early childhood on (Bogin 1999; Mei et al. 2004; Smith et al. 1976). This pattern, in which plasticity in many traits is greatest in early life, is widely prevalent across species (Bateson 2001; McCance 1962; Widdowson and McCance 1960). Such “developmental plasticity” is certainly one way in which phenotypic variability is shaped by ecological stresses. In humans, however, the primary period of plasticity occurs two decades prior to exposure to the adult environment, wherein many selective pressures relevant to reproductive fitness must act. This raises questions regarding the extent to which developmental plasticity in our species is indeed adaptive throughout the entire life course or under all ecological circumstances.
That human growth variability has an adaptive component over the short term is well established. In general, higher body weight at birth and during infancy is associated with greater survival early in life (Hogue et al. 1987; Kow et al. 1991; Victora et al. 2001), when extrinsic mortality risk is greatest. When nutritional supply is constrained, however, offspring grow slowly and appear to prioritize growth and development of some organs or body components at the cost of others (Hales and Barker 1992; Latini et al. 2004; Pomeroy et al. 2012).
The notion that early growth variability has long-term adaptive value is more controversial. If ecological stresses encountered in early life persist into later life, then developmental plasticity might promote fitness of the organism in its adult environment. For example, the thermal environment tends to be relatively consistent across broad global regions; hence, heat and cold stress early in life might induce beneficial adjustments in body size and proportions. Consistent with that hypothesis, ecogeographical analyses have demonstrated correlations of both adult phenotype and birth weight with heat stress (Roberts 1953; Katzmarzyk and Leonard 1998; Wells and Cole 2002; Wells 2012a), suggesting that human adaptation to the thermal environment begins in utero.
In volatile or unpredictable environments, however, deriving adult adaptation through early-life plasticity is inherently challenging. Paleoclimate evidence indicates that hominin evolution took place in increasingly stochastic environments (Bonnefille et al. 2004; Lisiecki and Raymo 2005; Potts 2012a, b; Trauth et al.
2005). Long-term “Milankovitch cycles” drive climate change over tens of thousands of years (Glantz 2001). Shorter-term climate cycles are also evident in the hominin paleoclimate record (Wang et al. 2008), including some that are analogous to contemporary El Nino-Southern Oscillation (ENSO) cycles (Hughen et al. 1999). These climate cycles, in turn, can be assumed to have introduced shorter-term ecological variability. Although phenotypic plasticity may potentially aid adaptation in such stochastic environments, developmental plasticity has a low degree of reversibility (Piersma and Drent 2003), and any adaptive benehts might not extend into adulthood.
This potential for “disconnect” between early-life plasticity and later-life adaptation is likely to have been exacerbated in recent human evolution by a substantial lengthening of the developmental period (Bogin and Smith 1996) which, paradoxically, may itself have been favored by stochastic environments (Wells 2012b). Whereas other female apes achieve reproductive maturity within a decade of birth (Galdikas and Wood 1990; Robson and Wood 2008), humans require around two decades to reach the same state. In volatile environments, this extended growth period decreases the likelihood that early plasticity will generate traits well suited to the ecological conditions encountered in adulthood. How then can developmental plasticity actually allow beneficial adaptation to the environment?
While ecological stresses may be evaluated in terms of direct, material environmental effects on growth, they may also be considered as a source of “information” about the quality of the environment with the potential to have more indirect, sustained effects (Bateson 2001). We can reframe the dilemma concerning timing of adaptive influences on developmental plasticity as follows: how might information received by organisms early in life be translated or processed in terms of adaptive growth patterns?