The new evolutionary synthesis: contents and summaries

Publication of Charles Darwin’s book “On the origin of species” in 1859 generated a revolution in biological science. The theory of natural selection (developed independently by Darwin and Alfred Russel Wallace) has provided a persuasive and robust explanation of evolution, especially since its linkage with genetic science in the 20th century (in what is known as the Modern Evolutionary Synthesis). A characteristic of the combined theory is that it predicts limits on how evolution can take place, not least in random genetic change being the sole source of biological variation. The phrase “nature not nurture” is often used to convey the idea that the nature of variations in form and function arising in organisms is not influenced by the environment. But recently cracks have started to appear in those prohibitions, and the consequences are profound and exciting.
Go to this page.

Here, we show an interesting exmple of animal biology that has contributed to the debate about the processes long assumed to drive evolution. It illustrates how new thinking was initiated regarding evolution’s mechanisms.
Go to this page.

Image credit:¹

Widely held assumptions about evolutionary processes are challenged in our first example. Though they existed for hundreds of millions of years, ammonites faced extinction several times. Their repeated survival involved biological memories of their evolutionary history acting as a resource for their recovery.
Go to this page.

Image credit:²

In this section we illustrate the kind of biological processes that ammonite atavism might have involved. This recently published work was a study of adaptation to high altitude in birds. In addition to researching the physiological adaptations enabling a strain of birds to thrive at very high altitude in Tibet the researchers sensibly examined what happens when they are exposed to the more abundant atmospheric oxygen concentrations at low altitude. The answer is that ancestral memory comes in useful. Physiological capabilities retained from their ancestral history as low altitude birds are redeployed, providing a source of the molecular processes required in the changed environmental conditions. One message from this work is that adaptations (the basis of evolution) needn’t always develop from new, novel variations in form or function; living things have sources of variation that are pre-existing and innate.
Go to this page.

Another butterfly example (see also the gaudy commodore and harlequin bug examples we show on our homepage) provides an introduction to the phenomenon of biological plasticity, where organisms can have different forms (phenotypes) depending on environmental conditions. Phenotypic plasticities are responses to normal environmental changes anticipated within the animals’ biology. But plasticity has a further capability – it also enables phenotypic adjustments to unexpected environmental circumstances. In doing this it provides evolution with a powerful tool.
Go to this page.

Image credit:³

Here we show how plasticity enables phenotypic adjustments to unexpected environmental circumstances. An American frog often exposed to pesticide pollution uses plasticity as a way to resist its toxic effects. Interestingly, though, this plastic effect is also generating permanent changes in the animal’s populations.
Go to this page.

Image credit:⁴

The wood frog example is one of plasticity in the animals’ biochemistry, but plasticity affects many aspects of phenotype. To illustrate this we describe an interesting case of a snake’s changing body shape.
Go to this page.

Image credit:⁵

At this point things become a little technical; it’s where we make some important conclusions that are inconsistent with the modern evolutionary synthesis.
Stay with us – it’s interesting.
Go to this page.

Image credit:⁶

Another example of adaptation to altitude demonstrates how completely new species can emerge from the adaptive capability of plasticity. The example is the Tibetan antelope (or chiru), a beautiful animal that is highly athletic at extremely high altitude. Evolution of this outstanding capability involved an intriguing change to the way the animal’s ancestors obtained sufficient oxygen in different conditions.
Go to this page.

Image credit:⁷

We have seen how plasticity is a mechanism of adaptation and consequent evolution. An example of a mechanism of how plasticity works (as opposed to what it does) demonstrates another departure from the classic, random genetic change based concept of adaptation. The progeny of zebra fish that have been exposed to oil pollution have a raised resistance to the pollutant’s toxic effects. In other words, the phenotypes of the progeny are dependent on the experience of their parents. Strikingly, that parental experience is not transmitted genetically. This example introduces the phenomena of epigenetics: mechanisms of heredity that demand extension of the evolutionary synthesis.
Go to this page.

Image credit:⁸

A recent study related to climate change further illustrates the inheritance of changes occuring to animals in response to unusual environmental conditions. This example suggests, once again, a form of adaptation that has not emerged from selection of random genetically based variation.
Go to this page.

Image credit:⁹

The long accepted mechanism of evolutionary adaptation is that natural selection acts on variations in form and function that are caused by random genetic changes. But here, in one of our most striking examples, we describe a case of environmental adaptation in an animal in the wild that has little to no genetic variation. This animal, a tiny invasive snail, presents a major challenge to exclusivity of genetic alteration as biological adaptation’s source of variation, and reinforces epigenetics as a mechanism through which responses to environmental demands can be transmitted to offspring.
Go to this page.

Image credit:¹⁰

The three previous examples demonstrate that environmental experience can be passed to animal progeny, setting up their biological constitutions to suit the conditions the parent encountered. This is contrary to past expectations, partly because of the difficulty of conceiving how information about animal bodies’ interaction with their environments could be transferred from their somatic tissues to their reproductive organs. This has long been inconsistent with known genetic and reproductive processes. Here we describe astonishing recent research that has demonstrated the flow of information from the body to the germline (reproductive organs), and a mechanism for it.
Go to this page.

Picture: Colour scan showing human liver (pink) and kidneys (red) in situ. Image credit:¹¹

For environmentally induced changes to phenotypes to become heritable it seems inescapable that there must be communication about them between somatic organs and the germline. We saw in the previous example compelling evidence of some kind of an information carrier transported by blood. In the mid 1990s some puzzling results from genetics research led to the discovery of a new class of molecules that may fulfil this soma to germline transport role.
Go to this page.

Image credit:¹²

The two previous sections introduced non-coding RNAs as a possible carrier of parental experience between somatic and germline cells. The question that follows is whether RNAs being transferred from soma to sperm are biologically active and, critically important, whether their effects are evolutionarily significant. A pair of studies on laboratory mice have demonstrated inheritance of induced behaviour, and that that inheritance is mediated by non-coding RNAs. This is an impressive case that clearly shows a potentially powerful way in which animals can adapt reactively and specifically, rather than only randomly, to environmental difficulty and opportunity.
Go to this page.

Image credit:¹³

The evolutionary synthesis is not limited to genetic and molecular mchanisms. We have seen how for a mechanism of phenotypic variation to contribute to evolution it must be hereditary. But not all heredity is genetic. Another form of heredity is culture (found in humans and non-human animals). The example of orca whale learning and behaviour illustrates how culture enables adaptation and is an evolutionary process.
Go to this page.

Image credit:¹⁴

Summary and context of the Darwin’s Loaded Dice message, and a hint of possible hope.
Go to this page.

Image credit:¹⁵