Should the genetic effects of environmental influences on phenotypes be paradoxical? It all depends.
Ghalambor et. al. have presented evidence for a case in which they are – those exerting adaptive influences on phenotypes constrain subsequent adaptive genetic evolution while those exerting maladaptive influences facilitate it – phenomena that Merila, commenting in the same issue, describes as “perplexing”. But should that always be the case? I doubt it. Instead, it should all depend upon whether the case is one of “genes as followers” or of “genes as leaders” (West-Eberhard 2003, Schwander & Leimar 2011).
Consider a property such as body length, one for which there is genetic variation for phenotypic plasticity in a population. A novel environmental influence appears which pushes body length, previously below the optimum for whatever reason, up towards or to the optimum, a push also enabled by one of those genetic variants for length plasticity in the population. That genetic variant would subsequently be favoured by selection over others. Analogously, if the environmental influence pushed body length beyond the optimum, the genetic variant enabling that would subsequently be disfavoured by selection. There would be nothing paradoxical in such cases – an adaptive environmental influence results in subsequent evolution for a genetic alternative and a maladaptive one in subsequent evolution against a genetic alternative. These are so because they are cases of “genes as followers”. The environmental influence was a novel one, one not common in the history of the species and therefore not one the genetic alternative had evolved by natural selection to respond to positively or negatively respectively in these ways or to this degree. They would be cases of Gould & Vrba’s exaptation in the one case (or nonaptation in the other); just ones with the added complexity that the genes involved are those for a plastic response. (Gould & Vrba explicitly limited their discussion to “a state of being” rather than “a process” but nevertheless commented “we might consider the flexibility of phenotype characters as a primary enhancer of or damper upon future evolutionary change.”)
On the other hand, consider a “genes as leaders” case. If the environmental influence was not a novel one but was fairly common in the history of the species i.e. one which the genetic alternative had evolved to respond to in that way, the story would be different. Then an adaptive environmental influence on a phenotype would not result in any subsequent genetic evolution. Subsequent genetic evolution would be “constrained” because the genetic alternative would have done just what it had evolved by natural selection in the past to do. A maladaptive environmental influence on a phenotype however would “potentiate” or “facilitate” subsequent genetic evolution, selecting against the alternative permitting an environmental influence to have such an effect. The evidence Ghalambor et. al. present pertains to Trinidadian guppies (Poecilia reticulata) and their interaction or lack thereof with predatory cichlids. The experimental evidence presented is too complicated to summarize here, but given the results showing genetic constraining and facilitating effects of plasticity, the case obviously falls into this second “genes as leaders” category.
One might be inclined to protest that the concept of “the reaction norm” of a genetic alternative is sufficient to deal with all such phenomena. But it is important that the concept of a reaction norm not be used in such a way as to make all cases of evolution ones of “genes as leaders” by definition. Surely not all parts of the ranges of all norms of reaction have been tested by natural selection.
Ghalambor, Cameron K., Kim L. Hoke, Emily W. Ruell, Eva K. Fischer, David N. Reznick & Kimberly A. Hughes. 2015. Nature 525: Sept. 17, 372-375.
Gould, Stephen J. & Elisabeth S. Vrba. 1982. “Exaptation – a missing term in the science of form” Paleobiology 8(1) 4-15.
Merila, Juha. 2015. “Perplexing effects of phenotypic plasticity.” Nature 525: Sept. 17, 326-327.
Schwander, Tanja and Olof Leimar. 2011. “Genes as Leaders and Followers in Evolution.” Trends in Ecology and Evolution 26: 143-151.
West-Eberhard, Mary Jane. 2003. Developmental Plasticity and Evolution. Oxford: Oxford University Press.