Epigenetics: the return of Lamarck? Not so fast!

I noticed that there’s a new book out by Peter Ward, a biology professor at the University of Washington who’s done a lot of work on nautilus cepalopods. (He’s also written several trade books in biology.) Here’s his new book, and, as you can see, the cover touts epigenetics as “Lamarck’s Revenge” (Jean-Baptiste Lamarck [1744-1829] was a French naturalist who proposed a theory of the inheritance of acquired characteristics.) The cover also promises to show how epigenetics is revolutionizing our understanding of evolution. Click on the screenshot to go to the Amazon site:

The book has been reviewed in several places, and I noticed that while it got a starred review on Kirkus, Publisher’s Weekly called it a “frustrating book” and has this in its review:

Ward references the classic study showing how starvation impacted one and perhaps two generations in the Netherlands following a WWII-era famine, but provides little hard evidence beyond that example. [JAC: see below for a discussion how even the famine study is flawed.] Without a proposed mechanism for such long-lasting effects and without data indicating such effects exist, Ward leaves readers with little more than suppositions.

And that’s the problem with the Lamarckian/evolutionary/revolutionary hypothesis. Environmentally induced changes to the DNA, usually produced by the placement of small methyl groups on DNA that affect what it does, are almost never inherited beyond one or two generations. This lack of stable change means that such environmental modifications cannot form the basis of permanent evolutionary adaptation. Ergo, it can’t revolutionize our view of evolution.  As the prescient Publisher’s Weekly reviewer noted, there’s just no evidence for the heritability of “Lamarckian” changes to the DNA.

I haven’t yet read Ward’s book, and don’t want to judge it by its cover, but the Nautilus site (the name is a coincidence, and that site was funded by Templeton) has reproduced an excerpt from Ward’s book, which is the article below on “fewer species”. Click on the screenshot to read it. And it gives me no confidence that Ward’s book presents a balanced view of epigenetics.

Lamarck’s Revenge, like David Quammen’s new book on phylogeny, seems to fall into the “Darwin was wrong” genre. (Darwin was supposedly wrong because modern evolutionary theory proposes that either mutations or genes transferred from other organisms are the variational basis for permanent adaptive change, and that the environment cannot itself influence DNA sequences in a permanent way. If environmental methylation did produce gene changes that could be both inherited and adaptive, and so spread through species, it would be a major change in how we view evolution.)

I should add that Darwin himself was “Lamarckian” because he thought the environment could somehow permanently modify heredity, and, as Matthew Cobb reminded me, Lamarck thought the changes occurred not through the environment, but through the animal’s “will.” Both men were wrong about heredity, but, as Matthew suggested, Ward’s book might better be called Darwin’s Revenge! After all, Darwin’s ideas were closer to these misguided epigenetic ideas than were Lamark’s theories.

Click and read:

 

Now the title doesn’t say much about Lamarck or the “evolution revolution”, but the article itself does. The title itself refers to work that Ward did with his colleagues on two species of Nautilus. One species, N. pompilius, occurs widely across the Pacific, while the closely related species N. stenomphalus is found only on the Great Barrier Reef. They were distinguished as different species by differences in morphology: they differ in whether they have a hole through the center of their shell, as well as showing big differences in both internal and external anatomy.

Ward, however says that they aren’t separate species because their DNA was identical using DNA-sequencing analysis (my emphasis):

We caught 30 nautiluses over nine days, snipped off a one-millimeter-long tip of one of each nautilus’ 90 tentacles, and returned all back to their habitats alive (if cranky). All the samples were later analyzed in the large machines that read DNA sequences, and to our complete surprise we found that the DNA of N. pompilius and the morphologically different N. stenomphalus was identical. No genetic difference, yet radically different morphology. The best way to interpret this is to go back to one of the most useful analogies in evolution: of a ball rolling down a slope composed of many gullies. Which gully the ball rolls down (corresponding to the ultimate anatomy or “phenotype” of the grown animal) is controlled by the direction of the push of the ball. In evolution, the ultimate morphological fate of an organism is caused by some aspect of the environment the organism is exposed to early in life—or, in the case of the nautiluses, while they slowly develop in their large egg over the course of an entire year before hatching. Perhaps it is a difference in temperature. Perhaps it is forces that the embryo encounters prehatching, or when newly hatched, the small nautiluses (one inch in diameter, with eight complete chambers) find different food, or perhaps they are attacked and survive, i.e., have two different kinds of predators. That’s why N. pompilius and N. stenomphalus are not two species. They are a single species with epigenetic forces leading to the radically different shell and soft parts. Increasingly it appears that perhaps there are fewer, not more, species on Earth than science has defined.

Well, the differences might not be genetic, but they might not be epigenetic either: the environment could simply change the development of the organism in different places without methylating or modifying its DNA in a heritable way, just as a plant given lots of fertilizer in one plot will grow taller than a plant grown without fertilizer in another plot. There’s no indication here that the differences in morphology of the two Nautilus species are caused by methylation of the DNA or histones, or by small RNA molecules—the three ways Ward says the environment might modify genes in a permanent way.

More important, when I looked up the paper on which this statement was based, I found, contrary to what Ward implied, they didn’t look at a lot of DNA in the two species, finding it identical. The paper (click on screenshot below), published in 2016, looks at only two genes in the mitochondria, and none from the nucleus:

An excerpt from the paper above:

Here, we report the genetic analysis of mitochondrial genes cytochrome c oxidase I (COI) and 16S rDNA, commonly utilized genetic tools for the phylogeographical studies of marine invertebrates, including cephalopods (Anderson 2000; Anderson et al. 2007; Dai et al. 2012; Sales et al. 2013a) from individuals across the known locations of Nautilus populations (Philippines, Fiji, American Samoa, Vanuatu, and eastern Australia – Great Barrier Reef). We chose COI and 16S because of their variability and success in past studies, and to align with sequences generated for this study with previous nautilus studies (Bonacum et al. 2011; Williams et al. 2012). We neglect nuclear genes (e.g., 28S or histone 3) because sequencing efforts have been limited in nautilus, precluding comparative analysis with past studies, and have been shown to be relatively uninformative for phylogenetic studies within this genus (Wray et al. 1995).

Now while the two species might indeed be one, you can’t conclude that from the identity of just two mitochondrial genes. And the Nautilus article at the top implies that a lot of DNA was examined. There may be substantial differences in other parts of the DNA that produce the morphological differences between the two (ergo these differences having a genetic rather than an epigenetic basis), and may even lead them to be reproductively isolated, ergo being two biological species.

I may have missed another paper looking at whole-genome sequences, but I doubt it. To me it seems that Ward is exaggerating his findings, and also implying that they extend to many species on earth, which might not be “biological” species because their differences are based not on DNA, but on developmental differences induced by the environment (and perhaps inherited via methylation). That might be true, but it’s an unwarranted extrapolation from a study of one organism.

Now Ward does mention one well known and important epigenetic property: the development of different cells and tissues in a single organism is often set off by epigenetic modifications that are themselves coded in the genome (i.e., the DNA of gene A says, “turn on/off genes B, C, D, and E under different internal environments”). Those differences are inherited through different cell divisions, which explains why, though all the cells in the body are genetically identical, they do different things and form different tissues. And those epigenetic changes are coded into the organisms’s DNA; they don’t come directly from the environment.

But that applies only to development of a single organism. It’s a very different thing to claim that environmental modification of the DNA of an organism is passed on through its gametes to its children, grandchildren, and so on, for that’s the only kind of environmental modification that can be involved in evolution. And the evidence says that this isn’t likely to happen. As I’ve said  repeatedly, methylation changes (and Ward notes this) are usually wiped out completely when gametes are formed, and we know of NO adaptation that is caused by environmentally-induced methylation of DNA or histones.

Yet in his popular article, Ward goes on to imply that this really does happen, and happens in human evolution as well. Here are a few excerpts (my emphases):

The methyl molecules are not physically passed on to the next generation, but the propensity for them to attach in the same places in an entirely new life-form (a next-generation life-form) is. This methylation is caused by sudden traumas to the body, such as poisoning, fear, famine, and near-death experience. None of these events come from small methyl molecules, but they cause small methyl molecules already in the body to swarm onto the entire DNA in the body at specific and crucial sites. These acts can have an effect not only on a person’s DNA but on the DNA of their offspring. The dawning view is that we can pass on the physical and biological effects of our good or bad habits and even the mental states acquired during our lives.

This is a stark change from the theory of evolution through natural selection. Heritable epigenetics is not a slow, thousand-year process. These changes can happen in minutes. A random hit to the head by an enraged lover. A sick, sexually abusive parent. Breathing in toxic fumes. Coming to God in religious ecstasy. All can change us, and possibly change our children as a consequence.

There is not a lick of evidence for any of that!

And there’s this:

. . . It has long been “truth” that the epigenome (the complement of chemicals that modify the expression and function of the organism’s genes, such as the methyl molecules that can glom onto specific genes during the life of the organism due to some environmental change) of the parent is reprogrammed (all epigenetic traces removed) twice: once during the formation of the gamete itself (the unfertilized egg, or a sperm waiting around to fertilize an egg) and secondly at conception. Erase and erase again. But now experiments definitively show that some of the chemicals added during the life of an organism do leave information in such a way that the offspring has [sic] their genes quickly modified in the same way that the parents did. The same places on the long DNA molecules of the newly born (or even the “not-yet” born) get the same epigenetic add-ons that one or both of the parents had. This is not supposed to happen. The revolution is the realization that it does. It happened to the nautilus. And it happens to you and me.

That is a gross exaggeration, and greatly misleading. If you want to see a good consideration and critique of the purported evidence for transgenerational epigenetic inheritance in humans, read this 2018 Wiring the Brain website post (click on screenshot) by Kevin Mitchell (note: he considers the overblown “Dutch famine” data as well):

Mitchell’s conclusion:

In my opinion, there is no convincing evidence showing transgenerational epigenetic inheritance in humans. But – for all the sociological reasons listed above – I don’t expect we’ll stop hearing about it any time soon.

He’s right on both counts: the evidence is horribly weak, and yet we still keep hearing about “Lamarckian” epigenetic inheritance, this time from Ward. After all, the message “Darwin was right” doesn’t sell books, but, in book publishing, “Darwin was wrong” is the scientific equivalent of “man bites dog”

As it says at the bottom of Ward’s article, these passages are from Lamarck’s Revenge. That doesn’t bode well for the book.

h/t: Nilou