“Beyond DNA: integrating inclusive inheritance into an extended theory of evolution”

CITATION:
E. Danchin et al. 2011. Nature Reviews Genetics, vol. 12, pp. 475-486.
ON-LINE AVAILABILITY:
ABSTRACT:
Many biologists are calling for an ‘extended evolutionary synthesis’ that would ‘modernize the modern synthesis’ of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.

THIS POST IS PART OF OUR ANTHROPOCENE BIOSPHERE PROJECT–A SERIES OF POSTS ON ERLE ELLIS’ ‘ECOLOGY IN AN ANTHROPOGENIC BIOSPHERE‘ (ECOLOGICAL MONOGRAPHS, 85/3 (2015))

The vast bulk of the impact that human beings have made on this planet has undoubtedly resulted directly from socially transmitted knowledge.

This quote, from Odling-Smee and Laland (2012), is one of several Ellis starts out with to set the tone for his article. It refers to the role of human culture, and especially to socially transmitted knowledge. Social transmission of knowledge (both horizontally, within one generation, and vertically, to the next generation) is clearly a hallmark of the human species. One of the first books to recognize this, Boyd and Richerson’s Culture and the Evolutionary Process, came out in 1985. This book was formative for numerous studies of social influences on many aspects of the behavior of humans and other animals.

Ellis certainly draws on Boyd and Richerson, but a major input to his thinking about evolution are ideas on “inclusive inheritance,” recently proposed by the French biologist Étienne Danchin and his colleagues. The theory of inclusive inheritance expands beyond the transmission of traits from one generation to the next by the passing on of genes. It looks at other avenues by which traits in one set of animals get passed on to others, including:

  • epigenetic inheritance (which has to do with variations in which genes get expressed or not),
  • ecological inheritance (very similar to niche construction—the process by which changes one generation makes in its physical environment to make it more suited to its needs become the given environment into which the next generation is born, and hence which exerts selective pressure on that and succeeding generations) (see Note 1 below)
  • cultural inheritance (the behaviors that members of a generation learn from other individuals, e.g. their parents and other members of the population to which they belong)

Danchin et al. thus take a holistic approach, in which they focus on information. Thus, even in the case of genetic inheritance it is not, strictly speaking, the genes that are transmitted, but rather the information that the genes encode. Likewise, the other mechanisms they discuss are passing on information the organism “uses” in its development to take on its phenotype (which includes both its physical properties and its suite of behaviors).

Danchin et al. offer a unified framework for understanding inheritance, one which places the kind of cultural transmission of niche construction skills Ellis talks about into a broader, biologically grounded (Darwinian), account of change across time. However, by stretching it across different mechanisms, they make their concept of inheritance less precise than it should be. Thus, even though their account is intuitively appealing, their concept of inheritance is being actively discussed but is far from universally accepted (see, e.g., Fellous et al. 2011).

I think that a possible source of confusion in Danchin et al.’s theory has to do with the question of the unit of selection. For practical purposes we typically assume that natural selection acts on individuals. Actually, genes are being selected, but for most traits the individuum hosting the genes is a very good approximation. Behavioral traits, including the traits leading to human culture and cultural evolution, need to be beneficial at the level of the individuum to be favored by selection. The effects of such individual behaviors can be viewed at the level of the population or species, but the unit of selection is still the gene. Essentially, there is a lot of doubt among biologists as to whether there is “group selection”—i.e. whether a trait will survive that is beneficial to a group independently of its benefits to the individuals who manifest it.

Think for example about a group that, to conserve its resources, limits its members’ reproduction to two offspring. Can this be evolutionarily stable? The answer is no. Just imagine a defector who decides to break the rules and have more than two offspring. The genes left behind by this individual will spread through the population, replacing the genes of the more responsible individuals. It would be better for the group if this didn’t happen—but in fact the effects of group selection are viewed as weak compared to individual selection.

I do not assume that Danchin and colleagues advocate for group selection, but with information as the unit of selection there is more room for confusion. Information is not a unified measurable entity. It can come in the form of what Danchin (2013) refers to as its physical “avatars:” DNA, RNA, numbers, letters, etc. If it is not clear what units are actually transmitted, it is also difficult to know how selection can operate on those units.

Despite my concerns, Danchin et al. help us understand Ellis’ project of synthesizing theoretical accounts of culture and of niche construction. Undoubtedly human culture is almost synonymous with humans constructing their own niche. While many organisms are capable of niche construction, humans are unique in the scale of their impact on their environment. Without that ability we would not be talking about the Anthropocene. But arguably the most profound effects we have on our globe is via one particular aspect of our culture, our economic system. This is obvious on many different levels, from burning fossil fuels to moving around invasive species by ship (Helmus et al. 2014). And it is obvious that financial markets play a key role in driving specific environmental changes (Galaz et al. 2015). But do we have good theory that connects evolutionary biology, culture and economics, beyond the obvious?


Note 1: Human beings pass on an ecological inheritance to other species, and thus become an agent of their evolution on many different scales. We are inducing evolutionary change in other species through global climate change, domestication, direct selection via hunting and fishing, manipulating ecosystems, to name but a few processes. And in a feedback loop of maladaptive niche construction we are in turn changing the evolutionary conditions for us, too. Just think about the recent panic surrounding the Zika virus: humans moved both the virus and the vector to the Caribbean, Central, and tropical South America, and climate change likely will help them spread into the US. (I have discussed this general phenomenon in a previous post.


FURTHER READING:
Boyd, R., and P. J. Richerson. 1985. Culture and the evolutionary process. University of Chicago Press, Chicago, Illinois, USA.
Danchin, É. 2013. Avatars of information: towards an inclusive evolutionary synthesis. Trends in Ecology and Evolution vol. 28, pp. 351–358. DOI: http://dx.doi.org/10.1016/j.tree.2013.02.010.
Fellous, S. et al. 2011. Adaptation due to symbionts and conflicts between heritable agents of biological information. Nature Review Genetics doi:10.1038/nrg3036-c1.
Galaz, V. 2015. Why Ecologists Should Care about Financial Markets. Trends in Ecology & Evolution vol. 30, no. 10, pp. 571-580. http://dx.doi.org/10.1016/j.tree.2015.06.015.
Helmus, M.R. et al. 2014. Island biogeography of the Anthropocene. Nature vol. 513, pp. 543-547. DOI:10.1038/nature13739.
Odling-Smee, J., and K. N. Laland. 2012. Ecological inheritance and cultural inheritance: What are they and how do they differ? Biological Theory vol. 6, pp. 220–230.
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3 thoughts on ““Beyond DNA: integrating inclusive inheritance into an extended theory of evolution”

  1. Nice post Ingo- and you have picked a truly great subject: I am deeply moved by the Extended Evolutionary Synthesis (inclusive inheritance) – it really is a game-changer in evolutionary theory. I agree that it does make inheritance and evolution by natural selection MUCH more complicated. But I am convinced that it is a more robust portrayal of the evolutionary processes that act to produce phenotypic traits and behaviors, both for humans and for nonhumans. To be clear, I am also very convinced that multilevel/group selection is a more robust and required model of evolutionary processes acting on social species, especially on an ultrasocial species, like behaviorally modern Homo sapiens. Though group selection and inclusive inheritance theory are certainly not accepted by all evolutionary theorists, I think they are gaining ground and will ultimately become core principles of evolutionary theory.

    • What do you make of Ingo’s point about the unit of selection? Can selection on the abstract unit of information (whatever the identity conditions for that might be) be separated from selection on the physical avatar? (BTW, philosophers speak of the “type/token” distinction to capture the two levels Danchin has in mind–the information, and the physical entity that conveys it.)

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