Extended Heredity A New Understanding of Inheritance and Evolution

In my recent review of She Has Her Mother's Laugh, I mentioned how the concept of heredity has become ever fuzzier the more we have learnt about how traits can be passed to the next generation. We have come from a very gene-centric period in biology, but biologists Russell Bonduriansky and Troy Day are ready to shake up the field. Neither a Lamarckian redux nor an attempt to downplay the importance of genes, this book successfully argues that the time has come to take into account non-genetic forms of heredity. Along the way, they provide a very interesting history lesson on how we got here in the first place.

Now, to be fair, rebellious as this notion might sound, it is not entirely new. Bonduriansky & Day join a growing chorus of biologists who feel that genetic inheritance is not the whole story. Notable pioneers in this field are Eva Jablonka and Marion Lamb who have been beating this drum for a few decades now (see their books Epigenetic Inheritance and Evolution and Evolution in Four Dimensions, published in a second edition in 2014). They defined four ways by which evolution might act, while Bonduriansky & Day rather cut the pie in two and talk of genetic and non-genetic inheritance that together form the concept they christen “extended heredity”.

They also rather not raise the spirit of Jean-Baptiste Lamarck. Yes, they say, he was an influential thinker, but his ideas of inheritance of acquired characters only vaguely resemble our current understanding, and the word Lamarckian can have several meanings. So, as opposed to some others (see my review of Lamarck's Revenge), they steer clear of terms such as neo-Lamarckism. But clearly, there was a time when this kind of thinking was in vogue. How did the gene triumph?

Though this book is not a history lesson in the evolution of biological thought in the vein of Sapp’s Genesis: The Evolution of Biology, the authors nevertheless spend a few chapters examining how we got here. Obviously, there was a series of pivotal scientific discoveries: Mendel’s famous crossing experiments with peas (see Mendel's Legacy and Gregor Mendel), and the elucidation of the structure of DNA (see Watson’s DNA: The Secret of Life). But as the authors show, ideology and politics played just as big a role. There was an enormous backlash against the idea of “soft” heredity in the wake of the horrors unleashed in the communist USSR by the scientifically illiterate agronomist Trofim Lysenko (see for example Lysenko's Ghost).

All this crystallised into the school of thought that became known as the Modern Synthesis (see Evolution: The Modern Synthesis) that gave rise to for example Dawkins’s famous book The Selfish Gene. Non-genetic inheritance was completely off the table, and it is remarkable, with the benefit of hindsight, to read the adamant statements from influential researchers such as Theodosius Dobzhansky or Ernst Mayr that the environment has no way of influencing DNA.

So, what are these forms of non-genetic inheritance then? Obviously, there is epigenetics in the strict sense. The authors take the treatment of the technical details of DNA methylation, histone modification, and RNA inheritance a step up from Carey’s previously reviewed book The Epigenetics Revolution. There is the idea that learning and culture are a form of heredity (often put forward to explain how humans set themselves apart), and there is the influence of the microbiome, which also gets passed on through the generations.

But Bondurianksy & Day offer other fascinating observations. The external morphology of single-celled organisms seems to be copied as a template in an almost mechanical fashion, including “mutilations” that were inflicted experimentally. Egg cells contain molecules and organelles, and both their nature, quantity and location, and how they are divvied up during cell division, matters. Sperm cells have long been caricatured as DNA packages with outboard motors, but carry other factors including RNA. Some of this can even originate from extracellular vesicles that travelled through the body from elsewhere and can fuse with sperm cells before fertilisation. What I didn’t even know is that after fertilisation the first few cell divisions happen under what the authors call a parentally programmed autopilot before the embryo’s genome takes over. One particularly shrewd observation the authors make is that the genome cannot be the whole answer for the simple reason that since life’s emergence, transmission of genetic material has happened together with the required replication machinery: a membrane-enclosed cell with its highly structured cytoplasm and all the material that it contains.

The remainder of Extended Heredity discusses how these ideas can be incorporated into existing evolutionary theory and why it is important. They also dedicate a chapter to deal with oft-voiced critiques and another one to speculate how outstanding puzzles in evolutionary biology could be reconsidered through fresh eyes.

Much more research, both applied and theoretical, will be required before these notions will become part of mainstream biology. In that sense, biological theories are like big ships – changing course is a slow and time-consuming process. Extended Heredity puts itself in the vanguard of this effort and is therefore by definition not the final statement on this topic. No doubt some of the things suggested here will be refuted in years to come. But the book builds a convincing case that non-genetic inheritance both exists and matters. For what is an advanced topic, its treatment could have ended up obtuse and impenetrable to outsiders. Instead, Bonduriansky & Day have written a book of great clarity, and have done so with great care. Whether you are open to the idea of non-genetic inheritance or not, this thought-provoking book deserves a close reading.