Transgenerational Plasticity: Lamarck’s Redemption

Dust off any high school biology textbook, flip to the evolution section, and you’ll see the stoic, world-weary face of Charles Darwin, father of evolutionary theory. His book On the Origin of Species laid the foundation for concepts, such as natural selection, that shape how we understand evolution and species diversity today. Pair his work with that of Gregor Mendel, another biology textbook star, and you get what evolutionary biologists call “The Modern Synthesis” or the theory surrounding how we understand genetic-based evolution (Mayr, 1982).

Before Darwin’s theory of natural selection, there were other ideas about how to explain the diversity of species around us. One such theory was that of Jean-Baptiste Lamarck, a contemporary of Darwin. As opposed to Darwin, who argued that natural selection only allowed the fittest species with the most adaptive traits to survive and pass on those genes to the next generation, Lamarck believed that the experiences during an organism’s lifetime created “acquired traits” that were then passed on. This theory was called “Lamarckism” or “soft inheritance” (Jablonka & Lamb, 2008).

Let’s break it down with a classic example. How did the giraffe come to have such a long neck?

Darwin would argue that giraffes with short necks would not be able to reach the leaves of trees and therefore die without reproducing. Selection would favor giraffes with longer necks and the next generation would inherit the long neck gene from the survivors.

In contrast, Lamarck believed that giraffes with short necks would have to stretch to reach the leaves. Each generation, the trees would get taller and taller and the giraffes’ necks would get longer and longer as the giraffes passed on this acquired trait.

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Lamarck and Darwin’s theories in comparison [Source]
We can see some inherent flaws in Lamarck’s way of thinking. For example, following through with his logic, if you were to do bicep curls with only your right arm every day for the rest of your life, your children should also have huge right arms and wimpy left ones. An even more extreme example, if you somehow lost your right arm, your children should only have one arm too! Critics were quick to point out these shortcomings and Lamarckism was rejected as a plausible theory. Darwin’s theory of natural selection would reign supreme.

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Portraits of Jean-Baptiste Lamarck and Charles Darwin [Source]
Fast forward to the present. We are seeing a burst of new research and literature suggesting that the environment experienced by your parents (and even your grandparents and great grandparents) can affect your own traits or phenotype. This phenomenon is often called transgenerational plasticity (TGP) or “non-genetic inheritance” and has a distinct Lamarckian flavor to it.

One such form of transgenerational plasticity involves heritable epigenetic changes. That is, heritable changes in the expression of genes that are not explained by a change in the sequence of an individual’s DNA. These changes involve structures associated with DNA (such as DNA methylation or histone proteins) that modify how genes are expressed. They can respond to changes in the environment and can be passed down to offspring.

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The two main components of the epigenetic code. [Figure from Qiu, (2006)]
Think of it like this. Your DNA is a toolbox and your genes (specific DNA sequences) are the tools in the toolbox. Epigenetics doesn’t change what tools you have in the box, but can determine which tool you are using. If the world presents you with a screw, you need both the right screwdriver inside your toolbox (the right gene) and you need to be holding the screwdriver not, say, a hammer (epigenetic control of gene expression). Following through, your children would then inherit your toolbox (genetic inheritance), and you could also hand them the screwdriver specifically since you already know that is the best tool for the job (epigenetic inheritance).

There are a lot of cool examples of heritable epigenetics beginning to be uncovered across a wide variety of taxa. For example, plants exposed to herbivores had offspring that were better defended against those herbivores than those with parents who weren’t exposed (Agrawal, Laforsch, & Tollrian, 1999). Mice that were provided learning enrichment navigated mazes better and their offspring also learned the mazes faster even without their own enrichment (Arai & Feig, 2011) . In humans, higher levels of obesity and other health problems have been found in Dutch people whose grandmothers were pregnant with their mothers during the Dutch Famine in WWII (a multi-generational effect) (Heijmans et al., 2008).

We are now beginning to understand that transgenerational plasticity along with other forms of non-genetic inheritance, like cultural inheritance (transgenerational transmission of behaviors and ideas) and maternal/paternal effects (pre- and post-natal conditions of parents and its effects on developing offspring), may be important in ecological and evolutionary processes. Our strictly Darwinian Modern Synthesis may fall short. The environment does affect the traits passed onto offspring and the experience of our parents can affect our own, perhaps providing a “fast-track” way to evolve adaptively in response to the environment.

Conversely, we are now beginning to understand the potential downsides to this plasticity. What if your parents hand you a screwdriver, but the world has changed so that now there are only nails? There is a possibility for TGP to be maladaptive too (Ghalambor et al., 2015). This possibility may be particularly important in our rapidly changing modern world. Will TGP rescue species or accelerate their downfall in the face of climate change and other human induced changes?

Either way, it seems that TGP may be important. In fact, a new “Extended Evolutionary Synthesis” is being proposed as an alternative to the traditional “Modern Synthesis” by incorporating these ideas into how we understand evolution (Laland et al., 2015). Lamarck may not have gotten it entirely right, but we now know that there is a Lamarckian twist to our traditional Darwinian inheritance.

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Portraits of Jean-Baptiste Lamarck and Charles Darwin [Source]
Isabelle Neylan is a 2nd year PhD student in the Population Biology Graduate Group at UC Davis in Dr. Andy Sih’s and Dr. Jay Stachowicz’s labs. She is interested in questions surrounding transgenerational plasticity and its possible implications for ecology and evolution using intertidal marine invertebrates as a study system. 


Sources:

Agrawal, A. A., Laforsch, C., & Tollrian, R. (1999). Transgenerational induction of defences in animals and plants. Nature, 401(6748), 60–63. http://doi.org/10.1038/43425

Arai, J. A., & Feig, L. A. (2011). Long-lasting and transgenerational effects of an environmental enrichment on memory formation. Brain Research Bulletin, 85(1–2), 30–35. http://doi.org/10.1016/J.BRAINRESBULL.2010.11.003

Ghalambor, C. K., Hoke, K. L., Ruell, E. W., Fischer, E. K., Reznick, D. N., & Hughes, K. A. (2015). Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature525(7569), 372.

Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., … Lumey, L. H. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences, 105(44), 17046–17049. http://doi.org/10.1073/pnas.0806560105

Jablonka, E., & Lamb, M. J. (2008). Soft inheritance: challenging the modern synthesis. Genetics and Molecular Biology31(2), 389-395.

Laland, K. N., Uller, T., Feldman, M. W., Sterelny, K., Müller, G. B., Moczek, A., … Odling-Smee, J. (2015). The extended evolutionary synthesis: its structure, assumptions and predictions. Proceedings. Biological Sciences, 282(1813), 20151019. http://doi.org/10.1098/rspb.2015.1019

Mayr, E. (1982). The growth of biological thought: Diversity, evolution, and inheritance. Harvard University Press.

Qiu, J. (2006). Epigenetics: Unfinished symphony. Nature, 441(7090), 143–145. http://doi.org/10.1038/441143a

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