Extending Darwinism

Incubator / by Eva Jablonka /

Is there more to heredity, natural selection, and evolution than genes and DNA?

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In the 1990s the evidence that epigenetic variants can be transmitted between generations of organisms was rather sparse, but this is no longer true. Epigenetic cell inheritance has become a major topic in molecular biology, and more and more examples of transgenerational inheritance are emerging. Gal Raz and I recently went through the scientific literature and found more than a hundred well-documented cases. They include inherited differences in the cortex; the surface structures of the protozoan Paramecium; self-reproducing architectural variants of proteins (prions) in fungi; inherited variations in flower morphology and color; inherited diseases in rats, induced during pregnancy by administering one dose of a male hormone suppressor to their mothers; inherited heart deformities in mice that were associated with transmissible, regulatory small RNA molecules. Our list isn’t endless, but it shows that heritable epigenetic variations occur in all types of organisms and affect many different types of traits. Our findings may be the tip of a very large iceberg. The variations had certain stabilities — some lasting for many generations, some for only a few — and they involved several molecular mechanisms.

The mechanism about which we know the most is DNA methylation. Certain genes are “silenced,” or rendered inactive, when small chemical groups (methyls) bond to some of the Cs of the four-letter alphabet (TAG C) that encodes information in DNA. These are not mutations because the coding properties of these Cs do not change, and if methyls are removed, the genes can become active again. This is not only an epigenetic control mechanism but also an epigenetic inheritance system, since a gene’s pattern of methylation, and hence its state of activity, can be replicated and passed on to daughter cells.

One interesting and important discovery is that stresses — unusual conditions difficult for organisms to cope with, such as extreme heat, starvation, toxic chemicals, or drastic hormonal changes — are potent inducers of heritable epigenetic change. They can, for instance, alter patterns of methylation at many different DNA sites. Genomic stresses can have a similar effect, such as those from hybridization between plant species. Two recently formed natural hybrids between American and European species of the cordgrass Spartina had 30 percent of their parental DNA methylation patterns altered. This is an extreme example, but there are many others showing that stress conditions cause genome-wide effects and are sometimes associated with extensive changes in DNA sequences. It seems that stress can lead to a repatterning of the genome.

What does all of this mean for our view of heredity and evolution? The first implication is that when we see different heritable types in a population, we should not automatically assume they are genetically different; the differences may well be epigenetic. When they are, they might have been induced by environmental conditions. Unfortunately, at present we do not know how much epigenetic variation exists in natural populations, although botanists are beginning to study this in plants. If there is as much natural variation induced by environmental factors as lab studies suggest, then rapid evolutionary change could occur without any genetic change at all.

Further, induced and heritable epigenetic changes may guide genetic changes. Imagine that an environmental change repeatedly leads to a particular developmental adjustment — hot conditions induce thin fur in a population of mammals, for example. This epigenetic change could persist in the population until a genetic change occurred and rendered the thin-hair phenotype “inborn.” In this way induced phenotypic changes, including epigenetically heritable ones, may precede and direct the selection of genetic changes. As Mary Jane West-Eberhard has aptly put it, “Genes are followers in evolution.”

In the light of epigenetics, old views of macroevolution must change. If wide-ranging epigenetic and genetic changes occur in stressful conditions, they are likely to have many effects on an organism’s form and function, its phenotype. This implies that conditions requiring novel adaptations to cope with them are often the very same ones that spur the massive epigenetic and genetic alterations conducive to rapid evolutionary change. A firm linkage between the production of new variation and its subsequent selection, something forbidden within the MS, grows ever clearer.

My colleagues and I have argued that various types of epigenetic inheritance have played key roles in all the major evolutionary transitions. For example, the symbiotic relations with bacteria that gave rise to modern cells would have been impossible without epigenetic mechanisms allowing their cell membranes to reproduce; cellular epigenetic inheritance mechanisms were necessary for the transition from single-celled creatures to complex multicellular organisms with many cell types; a new non-genetic system of information transmission (symbolic language) was crucial for the transition to human culture.

There is no doubt that acknowledging epigenetic inheritance alters our perspective on heredity and evolution. It eliminates the “negatives” in the MS and produces a broader theoretical framework, which puts the development horse firmly in front of the genetic cart. The origin of phenotypic variations takes a central position, sudden generational evolutionary changes assume significance, and soft inheritance gains recognition as part of heredity and evolution. Once again, Darwinian evolutionary theory is extending its boundaries and inspiring new studies that will further enrich our understanding of life, its history, and its future.

    Darwin 200More From Our Darwin 200 Celebration.

Originally published January 6, 2009

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