Extending Darwinism

Incubator / by Eva Jablonka /

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

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Courtesy Bitforms Gallery, NYC (detail of “Path 25, 2001” by C.E.B. Reas)

Like Charles Darwin, Jean-Baptiste Lamarck suggested that living organisms are products of a long process of transformation. But instead of asserting, as Darwin did, that diversity emerges through the natural selection and accumulation of heritable variations over time, Lamarck proposed two mechanisms of evolutionary change: an inherent tendency in living matter to become increasingly more complex and the inheritance of acquired characteristics — environmentally induced or learned individual adaptations that accrue over time and pass to offspring. Many biologists at the time, including Darwin himself, believed such “soft” inheritance was complementary to the theory of natural selection.

Soft inheritance was passionately debated for decades but fell from favor in the 20th century with the forging of the Modern Evolutionary Synthesis (MS), a version of Darwinism that unified the theory of natural selection with Mendelian genetics, and, later, the myriad discoveries from the midcentury molecular biology revolution of the 1950s, ‘60s, and ‘70s. For the past 60 years, it has provided the theoretical basis for evolutionary studies.

In the MS, Lamarck’s soft inheritance is effectively impossible. It explains biological heredity only in terms of the blind variation of genes (which are DNA base sequences). Gene exchange through either sexual production or some rare genetic mutations accounts for inherited differences between individuals; any and all bodily changes acquired or induced during an individual’s lifetime, such as muscles enlarged through exercise, cannot be passed to offspring. Macroevolutionary changes (such as new species) are simply the gradually accumulated effects of genetic variations; sudden evolutionary changes are rare and insignificant.

I and several other biologists believe the MS is in need of serious revision. Growing evidence indicates there is more to heredity than DNA, that heritable non-DNA variations can take place during development, sometimes in response to an organism’s environment. The notion of soft inheritance is returning to reputable scientific inquiry. Moreover, there seem to be cellular mechanisms activated during periods of extreme stress that trigger bursts of genetic and non-genetic heritable variations, inducing rapid evolutionary change. These realizations promise to profoundly alter our view of evolutionary dynamics.

Collectively, the processes that we believe have been neglected in evolutionary studies are known as epigenetic mechanisms. Epigenetics is a term that includes all the processes underlying developmental flexibility and stability, and epigenetic inheritance is part of this. Epigenetic inheritance is the transmission of developmental variations that have nothing to do with changes in DNA base sequences. In its broad sense, it covers the transmission of any differences that do not depend on gene differences, so it encompasses the cultural inheritance of different religious beliefs in humans and song dialects in birds. It even includes the developmental legacies that a young mammal may receive from its mother through her placenta or milk — transmitted antibodies, for example, or chemical traces that tell the youngsters what the mother has been eating and, therefore, what they should eat. But epigenetic inheritance is commonly associated with cellular heredity, in which differences that arise among genetically identical cells are transmitted to daughter cells.

Biologists have long suspected that mechanisms for epigenetic cell heredity must exist. Take, for example, our own embryonic development, when cells assume different roles. Some become kidney cells, others liver cells, and so on. Although they have the same DNA, liver cells and kidney cells look different and have different functions. In biologist jargon, they have the same genotype but different phenotypes. Moreover, they “breed true”: Kidney cells generate more kidney cells, and liver cells generate more liver cells, even though the stimuli that induced the different phenotypes in embryonic precursor cells are long gone. There must be some epigenetic mechanisms to ensure that a cell “remembers” what it was induced to be and transmit this “memory” of its altered state to daughter cells. This much is obvious. But surprisingly, we now know that cellular epigenetic variations are transmitted not only within organisms, but sometimes also between generations of organisms, via their sperm and eggs.

So if cells pass on information in epigenetic memories as well as in their DNA sequences, how are the two types of inheritance related? Marion Lamb and I have hit upon a helpful analogy. An organism’s genotype (DNA) is like a musical score; phenotypes are particular interpretations and performances of that score. Like DNA’s replication, a score can be copied and transmitted from generation to generation through high-fidelity duplication processes, and although small mistakes (mutations) crop up from time to time, the score remains essentially unchanged. But nowadays music is not transmitted solely through the score: Interpretations can be passed to future generations using the very different technology of recording and broadcasting (analogous to epigenetic inheritance mechanisms). Even with identical musical scores, performances differ, since they depend on the culture, conductor, musicians, and instruments. In the same way, DNA ‘s performance depends on conditions within the cell. Because of recordings, the musical interpretations of one generation may influence the subsequent performances of later generations. Similarly, because of epigenetic inheritance, the characteristics acquired in one generation can affect what happens in the next. Interesting interactions can occur between the two routes of music transmission — changes in the score will obviously affect the performance, but some performances may actually modify the score that later musicians use. There are comparable interactions between genetic and epigenetic inheritance.

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