Increasingly, researchers are beginning to argue that environmental heterogeneity and long-term ecological stochasticity have sculpted a remarkable breadth of phenotypic plasticity as the primary means by which humans have succeeded in replicating their genetic material^1,2. Variation in phenotypic response, it is argued, represents an adaptive solution to the problem of environmental unpredictability. Whether or not this is so is a matter to be arbitrated by empirical results – that Homo sapiens have managed to find a place in nearly every ecological niche on the planet, from the freezing Canadian Arctic to the island tropics of the South Pacific, is highly suggestive in this regard. To some degree this phenotypic flexibility is observable in physiological responses like shifting adiposity and skin tone³, though it is likely the expansive behavioral repertoire of humans provides the largest range of adaptive flexibility⁴. Humans cultivate social networks that ease energy flows and mitigate the reproductive costs experienced by females, who typically bear the brunt of the child-bearing load,  accumulate and modify trans-generational stores of information, use and invent tools to access previously unattainable resources, and play an active role in constructing the niches they inhabit^5,6. Of course, genetic variation stills plays a role in human evolution, as illustrated by the changes that facilitate adult lactase persistence in populations with long histories of animal husbandry⁷. Yet it is becoming more and more evident that the primary aspect of human variation responsible for our adaptive diversity is rooted in the dynamic interplay among genetic, cultural, and ecological systems of inheritance.

Once thought to be something of an evolutionary novelty, phenotypic plasticity is now understood to be extremely common and widespread. In environments characterized by consistent spatial and/or temporal heterogeneity, phenotypic plasticity can evolve as an adaptive response to variation in selection pressures^8,9. However, there is some debate concerning what exactly constitutes adaptive phenotypic plasticity and what selective pressures drive its evolution. Additionally, the apparent utility of plasticity in securing positive fitness outcomes across variable environments raises the question of why it is not a ubiquitous feature of all organisms across all environments. Adaptive plasticity can be identified where a single genotype expresses a range of phenotypes across a range of environments, provided that the range of phenotypes is shown to be heritable⁸. This, of course, leads a small definitional problem: establishing the boundary at which a single genotype begins and another ends is an arbitrary matter. At this point, it is unclear how well certain aspects of human variation meets this particular criterion. Phenotypic traits like adiposity and skin pigmentation show some level of heritability^10,11,12 (not a qualitative assertion – there is no reason to assume this should have sociological consequences, because race, as it is popularly construed, is a social construct). If this is so, these traits would be removed from the running as plastic responses in the strictest sense, since it is a rigid – rather than a plastic – response that is inherited. However, if we take the entire human genotype and the range of phenotype it produces the fact that only 6% of identified genetic variation is between sub-groups seems to indicate that, as a species, humans are pretty damn plastic after all¹³. Again, we return to the problem of definition: what counts as a single genotype?

Barsh, G.S. 2003

Selecting for Plasticity

Phenotypes are said to be plastic when a single genotype is seen to express multiple phenotypic states (reaction norms) across heterogeneous environments due to cues associated with the variable biotic and abiotic inputs present in said environments⁹. While one might be intuitively inclined to assume that this plasticity of phenotypic expression is a consequence of the pressures associated with environmental heterogeneity selecting for trait plasticity, this might not necessarily be the case. The observed plasticity could be a byproduct of some other trait, itself not directly connected to fitness outcomes^8,14. For the phenotypic plasticity to be considered an adaptive trait, it must be heritable and consistently associated with positive fitness outcomes. Consequently, adaptively plastic traits should evolve in environments characterized by long-term regularity in heterogeneity. That is, relative to the lifetime of any individual, the environment(s) experienced should exhibit some degree of variability or stochasticity, but with respect to the lifetimes of multiple generations of the same organism, the heterogeneity must be encountered consistently.  Conceptually, adaptive phenotypic plasticity is the product of the same forces that produce adaptation in any other trait, with the addition of multi-generational stability in environmental heterogeneity as a condition defining selection for adaptive plasticity.

The selective conditions that produce adaptive plasticity are those that consistently (over multiple generations) sort phenotypes (and the underlying genotypes) in such a way that plastic phenotypes show a higher fitness than alternatives. Put more simply, environments where adaptive challenges vary over differing temporal and spatial scales select for phenotypic plasticity. If this is so, we arrive at the question of whether or not the environments in which humans evolved meet these criteria. Growing evidence from paleo-climatological, archaeological, and paleontological research indicates that the environments experienced by our hominid ancestors throughout much of the Plio-Pleistocene – roughly the last 5 million years – were characterized by just the sort of climatic variability that would have made the more malleable bipedal apes the more fit^1,2,3,15. So, with regard to the proper evolution history – statistically significant pressures associated with a fluctuating climate – humans seem to measure up the strictures associated with the evolution of phenotypic plasticity.

Donges, J.F. et al. 2011 (24)

Demonstrating Plasticity

Though sometimes difficult to construct, experimental demonstrations of adaptive plasticity have been carried out. For example, density-dependent variation in stem elongation in response to light cues in the plant species Impatiens capensis¹⁶ and changes in morphology associated with the absence of predation cues in the fish species Poecilia reticulate¹⁷ have been put forth as experimentally supported demonstrations of adaptive phenotypic plasticity. The existence – or absence – of adaptive phenotypic plasticity is often examined through the use of reciprocal transplant (also known as common garden) experiments. In such an experiment, an organism from one habitat is placed in a different habitat in order to identify whether or not it responds plastically to the new conditions. If a plant has a plastic response to light cues, it should express different phenotypes in environments characterized by differing amounts of light exposure. Ideally, the variable of interest should be tightly controlled.

For human subjects, the ability to perform manipulative experiments like reciprocal transplantation is limited by practical and ethical constraints. Researchers can’t pluck a baby from a Boston hospital nursery and swap it with a child from the highlands of Papua New Guinea to see how they react. Fortunately, the range of habitats successfully colonized by human populations makes for an excellent natural experiment, allowing researchers to apply comparative methods to examine the relationship between phenotypic expression and environmental context. That humans not only inhabit, but in fact thrive in an immense range of habitats despite sharing the majority of their genes is good evidence that humans are adaptively plastic animals. This still leaves open the question of what governs of plastic responses. Multiple mechanisms of heritability have been proposed to account for adaptive plasticity, including allelic sensitivity, regulatory loci, and specific plasticity genes^14,18,  but the question of what genetic mechanisms ultimately underlie adaptive plasticity remain ultimately unresolved. For humans, it seems that the genetic architecture in question likely relates to our cognitive faculties – that is, the ability to search a landscape over the course of several generations and find adaptive solutions that are stored in an extra-genetic informational repository. That is, humans are species characterized by both genetic and cumulative cultural evolution.

Why Aren’t All Organisms Adaptively Plastic?

If organisms can evolve adaptively plastic traits in response to heterogeneous environments and nearly all environments exhibit heterogeneity on some spatial or temporal scale, this begs the question of why all organism do not exhibit plasticity in all traits¹⁸. Multiple answers can be found in the relative inflexibility of net fitness reaction norms (the most frequent response to a given environment)¹⁹, due in part to the frequently continuous nature of environmental variation, as well as the functional inter-dependence of phenotypic traits. First, the fact that selection ubiquitously acts to optimize fitness in a given environment constrains variation in fitness¹⁸. Since environments experienced by organisms tend to vary incrementally from one extreme to another, plastic responses can only be adaptive in the subset of environments where their performance is superior to alternative responses and their heritability is high. That is, a plastic response can only exhibit higher heritability and fitness than alternatives under certain conditions. In a transitional environment, the heritability of the response will be low, while in an environment distinctly different from than in which the response is beneficial, heritability for that trait will be non-existent, minimizing or completely eradicating its net fitness advantage^19,20. Additionally, traits often exhibit some degree of inter-dependence. As a consequence, a plastic response that might otherwise be positive could be rendered deleterious as a result of associated changes in other important traits¹⁴. To some degree, adaptive plasticity may depend upon the functional independence of the trait in question, or at least on the relatively low impact correlated traits have on fitness outcomes.

Further limitations on the evolution of adaptive phenotypic plasticity can be found in the potential costs and limits imposed on plasticity by the environment in which the organism lives and the physical-chemical constraints levied by aspects of the organism’s physiology. Though their ultimate effect is the same (restricting the evolution and expression of adaptive plasticity) costs and limits differ in their functional mechanics²¹. Costs operate by decreasing the fitness of phenotypes, while limits prevent the development of a plastic phenotypic response in the first place. Maintenance costs, for example, detract from fitness in instances where the sensory and/or regulatory mechanisms upon which a plastic response depends are too energetically expensive. Lag time, on the other hand, imposes a limit on the expression of plasticity when the phenotype is unable to respond to environmental cues in a timely manner^18,22. Since they have not been fully measured experimentally, the costs and limits that have been proposed as restrictions on phenotypic plasticity remain largely heuristic devices.

Conclusion

Given a prolonged association between the plasticity of response and improved fitness in consistently heterogeneous environments, phenotypic plasticity can be adaptive. Human evolutionary history seems to present just such a scenario, with frequent climatic oscillations selecting for a phenotypically plastic animal. Following our dispersal out of Africa, the challenges posed by migration between and colonization of differing habitats would have further selected for a malleable behavioral repertoire. However, the evolution of phenotypic plasticity is often inhibited by the inflexibility of mean fitness reaction norms, along with the range of possible costs and limits imposed by environmental and physiological constraints. Potentially fruitful avenues of research lie in identifying the specific heritable (genetic) mechanisms underlying adaptive phenotypic plasticity and measuring the relative importance of the various costs and limits that have been proposed as mechanisms preventing adaptive plasticity from being characteristic of all traits. With regard to humans, a complete explanation will be dependent on an understanding of the interaction between both genetic and cultural systems of informational inheritance²³. Though the tractability (or lack thereof) of these questions can be discouraging, a full understanding of adaptive phenotypic plasticity depends on their resolution.

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