Posts Tagged ‘genes as leaders’
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.
In a previous post and elsewhere (e.g. here Biological Theory 2(1) 10-22 gated and here Spontaneous Generations ungated ) I suggested extending Van Valen’s definition of evolution to incorporate development and ecology and to acknowledge the fact that there are two distinct pathways to evolution by natural selection. New genes can reconstruct old environments or new environments can reinduce the expression of old genes or both, but even if both, one or the other is likely to lead and the other to follow initially. In an article this month (Trends in Ecology and Evolution V26#3 here), Schwander and Leimar call the first “genes as leaders” and the second “genes as followers”. P. Z. Myers once exquisitely analysed an experimental case on Pharyngula here (a case originally published by H. F. Nijhout in Science).
It is important that the possibility of “genes as followers” not be misunderstood as sneaking Lamarckian explanations for adaptation in by the back, or should I say by a side door! Environmental influences on phenotypes beyond the historically experienced range, just as novel genes expressing a norm of reaction beyond that historically expressed, are more likely to be maladaptive than adaptive – which is not to say that either cannot have a selective effect – albeit one usually negative, at least at first.
Now to the new development. Schwander and Leimar make the novel (but in retrospect obvious) proposal that which direction change has taken place in any particular case can be detected using phylogenetic methods. Recall that Darwin said that his theory of descent with modification was composed of two great principles – “the unity of types” (i.e. history) and the “conditions of existence” (i.e. natural selection). Since the work of Harvey and Pagel in the late 1980s and early 1990s, it has become common in evolutionary ecology, and even in some cases in anthropology, to control for the former in testing particular hypotheses about the latter. However such methods have never before to my knowledge been applied to this question.
Schwander and Leimar apply “ancestral state reconstruction methods” to the question of how commonly switches (and losses) have taken place between genetic polymorphisms and polyphenisms. They admit to many limitations of their study. They consider only discrete and not continuously varying characteristics. They use selected examples, i.e. the evidence is anecdotal. Nevertheless, by mapping genetic polymorphisms and polyphenisms (as well as losses) for the same phenotypic characteristics in the same larger group such as winged and winglessness in carabid beetle species and right and left handedness in Heteranthera plant species for example onto their phylogenies, they have begun to pave the way towards answering this fascinating question. Bravo!
From the series of examples considered, they conclude that there is “no clear tendency for genes to be followers or leaders overall”. However it is important to understand that an historical change to, does not necessarily mean a change by means of . An evolutionary change from a genetically polymorphic species to a polyphenic one could nevertheless have been initiated by a genetic mutation or recombination followed by selection for adaptive phenotypic plasticity under conditions of uncertainty but with reliable cues. However, given that virtually the identical alternative phenotype was present as a genetic alternative in the ancestral polymorphic species, it is more likely that the alternative phenotype was latent in the formation of the new species and came to be induced there at least initially by an altered environment. In other words, it was likely a change initiated by environmentally inductive means as well as a change to environmentally inductive control. Still, as the authors eventually make clear, “the frequency and direction of transitions between them depends not only on how often either system emerges but also on how often one system is more beneficial than the other. Polyphenism should be favoured when a phenotype-determining environmental cue accurately predicts the selective condition for which the corresponding morph is suited, whereas genetic polymorphism should be favoured when such environmental cues are lacking and there is local frequency dependence or spatial variation in conditions, combined with limited gene flow.”