Tinkering and timing in evolution

What’s in an embryo

Steven Jay Gould was a highly influential evolutionary biologist: among other important contributions to the discipline, he (with Nils Eldredge) developed the theory of punctuated equilibrium which, though controversial, was a new view of the way evolution takes place over time, and remains a prominent concept in the field. He was also a science historian and highly successful writer of both leading edge technical work and articles and books for non-specialist readers. The choice of subject for his first book, Ontogeny and Phylogeny¹, typified the versatility of his intellect. Ontogeny and Phylogeny was partly a history and reanalysis of an old, once prominent area of biology: the biological significance of features in embryos that are typical of adult animals of species other than that of the embryo itself. Examples include the asymmetric shapes of certain embryonic fish tails that resemble those of more evolutionarily primitive fish rather than the symmetrical tails their own (more complex) species have as adults. Fish are also ancestral to amphibians, and there is a biochemical resemblance between developing amphibians and adult fish. Fish excrete waste nitrogen as ammonia, and so do amphibian tadpoles, but only until metamorphosis to their adult form in which the nitrogen is excreted as urea.

These examples suggest some kind of connection between ontogeny (the course of development during organisms’ lifetimes) and phylogeny (the evolutionary history of organisms). During the nineteenth century the possibility that this connection was that the evolutionary history of species reappears as stages in their embryonic development (recapitulation) was an important area of research and debate. Though the recapitulation was discredited the idea remained influential and pervasive.

Gould’s book is a history of the relationship between evolutionary and developmental thinking in biology. In it he challenged the conventional view of evolution as a simple and linear process, and instead highlighted the complexity, diversity, and creativity of evolutionary mechanisms. A major part of this was a focus on heterochrony, the changes in developmental timing that can be a powerful mechanism in the evolutionary generation of new forms, and which helps to resolve the significance of ancestral resemblance during embryological development. Consequently, the book was influential in stimulating research into heterochrony, helping to create the field of evolutionary developmental biology.

Starting with what you have

Shortly before publication of Ontogeny and Phylogeny, in 1977 the great molecular biologist Francois Jacob challenged assumptions about exactly how natural selection operates as a creative process. In the 1960s Jacob, with Jacques Monod, identified how genes are controlled in bacteria, a hugely important scientific breakthrough. Molecular based gene regulation is now known to occur in all life-forms, and to be a fundamentally important component of all biological processes. That commonality influenced Jacob’s thinking on evolution. In his paper ‘Evolution and Tinkering’ ^{2 & see 3 & 4} Jacob argued that evolution is not free in the directions it can take. This is because the starting points of all evolutionary events are themselves biological entities, and their characteristics restrain what is evolutionarily possible. In other words, what evolution can do depends on what is already there; continuing evolution of biological entities (be they entire organisms, organs or cell signalling pathways) is constrained by the history of their evolution. To illustrate this consider the design of a car: it can be further developed into a van, something that happens regularly with modern cars. But it would be very difficult to develop a kitchen food mixer starting from the car’s design.

It turns out that using what already exists rather than creating biological material from scratch can be highly effective. For example, round about the time Jacob was writing, new research techniques were starting to reveal unexpected similarity between organisms at the molecular level. In 1975 it was discovered that 99% of the DNA that codes for proteins is the same in chimpanzees and humans. This was surprising, for it had long been assumed that the changes to characteristics that evolution involves resulted from changes to the genes directly coding for those characteristics, hence an expectation that genomes would differ substantially between different types of organisms. How the two species can be so clearly different with such minimal difference in their genetic material can be explained by genes being redeployed to different functions, and by changing the timing of their operation. Jacob suggested from this and other evidence that evolution takes place via a process resembling the French concept of bricolage, creation from a diverse range of things that happen to be available. He cited examples of biological characteristics that probably suggest bricolage in their evolution, arguing that such examples are common. Also, inter-species homology (e.g. the similarity of chimpanzee and human DNA and its explanation in gene redeployment) is evidence that bricolage is evolutionarily powerful: witness how different humans and chimpanzees are in appearence, function and how they live. Jacob’s argument was that the clear abundance of bricolage examples, and the strength of its evolutionary capability, mean that it is nothing less than a creative force in evolution. That suggestion is both profound and disruptive because it challenges a central aspect of the Modern Evolutionary Synthesis (MES), that natural selection is the sole creative force in evolution.

Influence

These two publications initiated new thinking about how evolution takes place, notably regarding the role of embryological development in evolutionary change, something that had been neglected in the MES. This seeded the emergence of evolutionary developmental biology (evo devo) as a research area. The publications also influenced a focus in genetics research that confirmed the idea of altered patterns of gene expression as an evolutionary mechanism. These ideas strained the reach of the MES and its implied assumption that the key mechanisms of evolution had been solved. A group of scientists developed this new view of the scope of the MES, arguing the need for an Extended Evolutionary Synthesis.

Image credits:
Left; H. Raab (User:Vesta), CC BY-SA 3.0 https://creativecommons.org/licenses/by-sa/3.0, via Wikimedia Commons
https://commons.wikimedia.org/wiki/File:Archaeopteryx_(Feather).jpg
Centre; Tylwyth Eldar, CC BY-SA 4.0 https://creativecommons.org/licenses/by-sa/4.0, via Wikimedia Commons
https://commons.wikimedia.org/wiki/File:Dinosauria_-_Archaeopteryx_03.jpg
Right; Extract from original image by Robert Thibault
https://uk.inaturalist.org/photos/339387419

References

1. Gould S.J (1977) Ontogeny and Phylogeny. Belknap Press, Cambridge, Massachussetts. [↩]
2. Jacob, François. ‘Evolution and Tinkering’. Science 196, no. 4295 (10 June 1977): 1161–66. https://doi.org/10.1126/science.860134. [↩]
3. Jacob, François. ‘Complexity and Tinkering’. Annals of the New York Academy of Sciences 929, no. 1 (April 2001): 71–73. https://doi.org/10.1111/j.1749-6632.2001.tb05708.x. [↩]
4. ‘“Evolution and Tinkering” (1977), by Francois Jacob | Embryo Project Encyclopedia’. Accessed 21 December 2023. https://embryo.asu.edu/items/172791. [↩]