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Dan Hartl, Sewall Wright, and the Role of "Ecological Opportunity" in Evolution

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As I wrote in a previous blog, I attended the EMBO conference "Evolution in the Time of Genomics" in Venice this past May. At that conference, after my presentation (visible on YouTube), I had an exchange with Dan Hartl, a Harvard evolutionary biologist who studies Drosophila.

I had emphasized invention and creativity in evolution. So Dan told the story of what happened when he asked one of the pioneers of the Modern Synthesis, the legendary population geneticist Sewall Wright, about where novelty arises in evolution.

"I want to tell a story. When I was a graduate student, I once asked Sewall Wright, who was a pre-eminent population geneticist, 'What limited novelty in evolution?' And he said, 'Novelties came about from ecological opportunity.'... But then he said, 'Unfortunately, you can't make a theory out of that, because these events tend to be irregular and unpredictable.' And what you need to make a theory is a reproducible series of events, so that you could test it. So population genetics was never designed to encompass all the things that you talked about -- it was designed for the conventional, reproducible parts of evolutionary biology."

In addition to supporting my point that we need to think about evolution as a complex process, Dan's anecdote raises an important subject I discussed in my book: the relationship between ecological change and evolutionary invention. Commentator Billll also raised this point in one of his comments to my blog on Symbiogenesis:

"Natural Selection ... imparts directionality only in the sense that the creation of a new ecological niche, after an ecological collapse perhaps, favours the selection of variants that can utilize the niche to increase their reproductive success."

All these comments make it necessary to discuss how ecological changes can influence evolution. From the conventional perspective, as articulated by Wright and Bill, natural selection only has an influence by providing opportunities for new adaptive features to provide reproductive advantages. If we think of variation and selection as the two pillars of evolutionary theory, ecology only affects selection in this view.

However, molecular analysis of genome regulation and change have uncovered additional pathways for ecological input into the evolutionary process. Recognizing that genome change is an active biochemical process ("natural genetic engineering") means that it is subject to cellular control circuits, in particular to epigenetic silencing. Thus, these control circuits are targets for ecological inputs, just like all aspects of physiology.

Ever since the work of Barbara McClintock , we have known that natural genetic engineering can be activated by various "shocks" and stress stimuli.

One of the most important classes of stress that activate genome change is hybridization between different populations or species. Although the subject deserves far more study, it is logical to assume that ecological collapse will deplete normal interbreeding populations and thus lead to a rise in unusual mating events. Since these are just the events that stimulate natural genetic engineering functions, we see that there are unexpected ways ecology can have a direct influence on the variation process as well as on selection.

We know from studies in Drosophila and plants that a major aspect of cell control over natural genetic engineering is RNA-targeted epigenetic formation of silent chromatin that inhibits the expression of mobile genetic elements. In keeping with this knowledge, it is important to note that hybridization and other stresses that lead to genome instability are also events that modify chromatin formatting. Thus, there is a solid molecular trail between ecology and genome change that experimentalists can follow.

The connection between ecological collapse and increased genome change has two important consequences for the evolutionary process. The first consequence is that evolution is an episodic process linked to changes in the ecology. It is not a continuous gradual process following Uniformitarian principles as Darwin argued.

Unpredictable disruptions to the ecology, as Sewall Wright pointed out, will lead to major episodes of evolutionary inventiveness. This happens in two ways: (1) directly, by stimulating change, and (2) selectively, by providing adaptive opportunities. The changes, by the way, may well include an increase in symbiogenetic events as well. We don't know whether that happens, but it is another potentially rich field for future evolution science research.

Wright's "ecological opportunities" have a second unexpected but potentially major impact on the evolutionary process. While ecological collapse imposes greater challenges and stresses on the organisms adapted to previous ecology (i.e. strengthens selective pressures), by depleting the overall density of life forms, it relaxes the selection on their offspring with novel adaptations to the new situation. This means that imperfect but functional novelties can provide important selective advantages before micro-evolutionary processes have had an opportunity to fine-tune them.

In other words, the connection between ecological collapse and episodes of rapid evolutionary innovation means that novelties with minimal functionality have a greater chance to become established than they do in a stable ecology. This is an fascinating aspect of episodic evolution that might be subject to real-time study in synthetic macrocosms.

One final aspect of the ecology-evolution connection has become current because of our increased knowledge of the molecular basis of epigenetic modifications. A key property of epigenetic controls is that they are heritable over individual cell generations, as in embryonic development, and even across organism generations in so-called "transgenerational" effects (Hauser, Aufsatz et al. 2011; Daxinger and Whitelaw 2012).

Since epigenetic controls are subject to ecological inputs and since heritable phenotypic differences are subject to natural selection, molecular studies of epigenetic formatting have stimulated Lamarckian interpretations of evolutionary changes (Gissis and Jablonka 2011). This is yet another way that molecular studies are carrying us farther from classical evolutionary theory and into a new realm of rapid scientific change.

Stay tuned and keep your hat on tightly. The ride is likely is to speed up.


Daxinger, L. and E. Whitelaw (2012). "Understanding transgenerational epigenetic inheritance via the gametes in mammals." Nat Rev Genet 13(3): 153-162.
Gissis, S. B. and E. Jablonka, Eds. (2011). Transformations of Lamarckism: from Subtle Fluids to Molecular Biology. Cambridge, MA, MIT Press. .
Hauser, M. T., W. Aufsatz, et al. (2011). "Transgenerational epigenetic inheritance in plants." Biochim Biophys Acta 1809(8): 459-468.