The new evolutionary biology

Table of Contents

Nature and nurture

The origins of living things, with their astoundingly diverse forms and functions, has fascinated thinking people since ancient times. Modern understanding of how evolution works arose from ideas conceived independently by Alfred Wallace and Charles Darwin, and famously developed by Darwin in his book, “On the origin of species1 published in 1859. The idea of living things changing progressively over time has existed since antiquity. Palaeontology and the idea of evolution as currently understood emerged in the 18th and early 19th centuries2. What Wallace and Darwin brought to the field was a credible mechanism for evolution: that small variations in the form and function of living organisms provide differences in their capability to survive and reproduce, leading to beneficial variations progressively increasing in frequency in populations in a process that Darwin termed “natural selection”. (“Survival of the fittest”, a phrase coined by Herbert Spencer3, captures the concept of natural selection effectively and has become a popular term for it.) Natural selection of variants and the adaptations they enable in living things is the basis of the emergence of species of organisms, their eventual extinction, and replacement by new ones.

“A problem for Wallace and Darwin was that neither of them knew what caused the variations to appear”

A problem for Wallace and Darwin was that neither of them knew what caused the variations to appear; understanding of that had to wait for the development of genetic science. The integration of natural selection theory with genetics during the first half of the 20th century provided a fuller and even more persuasive explanation of evolution: that the variations on which natural selection acts are caused by random physical, and consequently heritable, alterations to genetic material called mutations. This integrated mechanism (termed, The Modern Evolutionary Synthesis (MES))4 has repeatedly explained or been consistent with many phenomena observed in evolutionary research, and has long been widely accepted as the core mechanism of evolution.

An important consequence of the MES is the severe constraints it imposes on how variation and consequent adaptation of organisms can occur; it predicts that some processes are impossible, and this has long prevented serious consideration of them. However, powerful as the MES is, it is far from a complete explanation of how evolution works or, more generally, of the history of life. There is more to evolution than the MES; indeed, some biological phenomena are inconsistent with it, and this has stimulated alternative lines of research that have produced radically new knowledge and perceptions. One aspect of this concerns the links between environmental conditions and variation.  Darwin and other contemporaries suspected that the environment might cause or influence variation, but their reasoning was restrained by the mechanisms of cell biology, heredity and embryological development not being understood at that time. Mutational randomness is not affected by environmental conditions; the environment can exert natural selection on variations once they have occurred, but cannot affect the types of variations that are made available. That isolation, in the MES, of variation’s origin from the environmental challenges and opportunities that it addresses is sometimes expressed as the phrase, “nature not nurture”. Here, we show how this assumption is becoming inadequate and, in doing so, is generating an extended view in which evolution can respond to environmental threat; evolution still involves the throwing of mutational dice, but often their effects are loaded. Throughout, we base our description on interesting examples of animal adaptation, starting with an example from distant time.

Evolutionary history to the rescue

Given the scale of its meaning, era is a small word. Description of Earth’s history has to cover its 4.5 billion year existence, and in geological science that gigantic amount of time is divided into periods within which significant things happened to and on the planet. Eras apply to periods of several hundreds of millions of years. For modern humans, who have existed for only about 300,000 years and who usually live for less than 100, these time spans defy comprehension.

Eras are a useful division of time when considering the existence of groups of animals. Ammonites were molluscs, now extinct but widely recognized in the beautiful fossils formed from their spiral shells. These extinct cephalopods, a class of molluscs that includes modern octopus, squid, cuttlefish and nautilus (the latter of which they superficially resembled), lived from 409 million years ago (Mya) to 66 Mya. That 343 million year period spanned two geological eras, starting about half way through the Paleozoic and ending at the close of the Mesozoic. To put that into context, the dinosaurs evolved, lived and became extinct entirely within the Mesozoic era. So, in terms of how long they existed, ammonites were very successful, and that success is demonstrated by their diversity.

Image credit: Partonez, CC BY-SA 4.0 , via Wikimedia Commons
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Around 10,000 species of ammonites have been identified from their fossils. Probably, more than 10,000 actually existed, though not all at the same time; individual species arose and became extinct as the class continually evolved over its 343 million years. As they evolved, they developed great variety in their distinctively coiled shells. The shells varied in size between a few centimetres to several metres in diameter. They also differed in their features and shapes, with variation in external lumps, ridges and spikes, and in patterns of invagination on their septa (the walls separating the series of chambers of which the shells were constructed). Some ammonites weren’t even helical, having straight shells or ones that were only slightly coiled.
Ammonites as a group, then, clearly had an effective way of living which made them extremely successful. Despite this, they suffered disaster several times . Conditions on Earth alter profoundly during eras. Titanic processes such as vulcanicity cause changes to atmospheric oxygen concentration, sea levels and other environmental conditions that have huge, sometimes devastating, effects on living things. This happened to the ammonites which, during their time, experienced no fewer than four mass extinctions. How they survived and prospered after three of them is striking.

After each of the first three extinctions there appeared new ammonite species with notably small and simple shells5. Resembling the shells of long extinct ammonites, they were, at least morphologically, primitive. Prior to the extinction, each period of evolution had progressively generated ammonite species with increasingly complex shells. That elaborate morphology probably indicated specialisation in how individual species lived, the ecological niches they occupied, what they fed on, their defences against predation, and how they behaved.  Conversely, the simplicity of the new species that replaced them after mass extinction may well suggest that these were generalists rather than specialists, possessing flexibility that enabled them to live, for example, on varied types of food during times of scarcity. As evolution continued, these simple replacement animals gave rise to progressively more complex and specialised species as ammonite populations expanded and re-diversified into new and more niche environments.

“… there appeared new ammonite species with notably small and simple shells. Resembling the shells of long extinct ammonites, they were, at least morphologically, primitive.”

Animals that are simple and relatively non-specialised, and that maximise their chances of successful reproduction by producing large numbers of progeny, are often good survivors in difficult or changing environments. So the availability of simple forms of an animal group is therefore an important resource upon which evolution can act. Some groups may have small and simpler species already in existence,  contemporary with evolutionarily more advanced and complex relatives, prior to any challenge from serious changes in their environment. That was not the case for ammonites. The paper argues that the fossil record and other evidence show that the newly evolved primitive forms only appeared after the major ammonite extinctions had occurred; they were new species, not expanded populations of species that existed before the extinction events. The reappearance of evolutionarily primitive forms of biological characteristics is called atavism, and it appears that, several times, atavism resulted in these simple and versatile replacement ammonite forms, enabling them to adapt to and thrive in new environments, becoming new starting points for evolution to continue5. If we consider these atavistic events with reference to the MES we encounter a discontinuity.

The core of the current orthodox version of evolution is that random changes (mutations) in organisms’ genetic material (their genomes) cause variations to the forms and functions (i.e.  the phenotypes) of organisms. Those phenotypic variations (remember that in the MES model they have a random cause) may be beneficial or deleterious to individuals that have them in populations of species, consequently affecting their relative ability to survive and reproduce successfully, and for their progeny subsequently to survive and reproduce. Biologically, this comparative ability is known as “fitness”. Natural selection, then, is the process in which variations endowing higher fitness in comparison to others lead to their bearers dominating and eventually replacing compatriots lacking those variations. Progressively, repeated and cumulative iterations of that process generate substantially altered forms of organisms, and eventually their evolution into new species. Thus, variation in phenotypes is the raw material of natural selection and, (consequently) evolution. In the MES, the randomness of genetic variation is critical in generating multifariousness in the phenotypic variation that occurs.


But the repeated ammonite atavism is a phenomenon of similarity, not disparity, suggesting that there is more to the story than random processes. Evolution generated strikingly similar new ammonite species in response to three dissimilar, extremely severe environmental crises. This suggests that the atavistic processes behind those evolutionary similarities did not have an entirely random basis. Instead, they seem somehow to have been likely to occur; rather than being generated entirely from random variation, the capability to evolve in an atavistic direction appears to have been innate. The next section describes how this might have happened.

Biological memories of an ancestral environment

A recent research report reveals the kind of processes tha ammonite atavism might have involved 6. This research investigated how birds react to altitude. Domestic chickens were introduced to high altitude on the Tibetan plateau over 1000 years ago. As one might expect, the modern descendants of those pioneer birds have evolved adaptations enabling them to survive successfully at these very high elevations. For example, one adaptation to the low atmospheric oxygen levels (hypoxia) is a distinct form of haemoglobin in their embryos’ blood that is unusually efficient in carrying oxygen to their developing tissues. These adaptations are now innate to the high altitude birds; they are permanently present and heritable.

Chickens from low altitude areas are far less able to live in hypoxic conditions (for example their eggs have reduced hatch rates, and hatchlings have a low rate of survival to adulthood). Some survival is possible, however, due to physiological changes the low altitude chickens undergo when oxygen is low. Those changes are neither permanent nor hereditary, they involve a set of genes that change the degree to which they are active (i.e. their “expression patterns”) depending on the amount of available atmospheric oxygen.

The adaptations of the high altitude birds are mechanistically quite separate from the flexible physiological response of the low altitude birds to oxygen availability (they involve different genes). A fact that is perhaps surprising is that the high altitude birds, in addition to their unique, special adaptations to altitude, have retained the original system as well. Experiments have shown that, if eggs from high altitude birds are artificially transferred to low altitude conditions, the flexible system still reacts, setting the physiology of the embryos to the ancestral low altitude state. The high altitude chickens therefore have two biological systems for dealing with altitude: the original reactive one, and the more recently evolved one that provides their increased capability.

It appears that the flexible system adjusts to meet either low or high altitude conditions (albeit to a limited extent regarding the latter) suggesting that both oxygen abundance and deficiency present their own physiological challenges. Though the high altitude birds do not normally encounter abundant oxygen concentrations, they have retained an ancestral process in a dormant state and can reactivate it as a resource to adjust to a high oxygen situation when they are exposed to it. This, then, is a form of atavism that provides a resource when an environmental challenge resembles historical conditions.

”This, then, is a form of atavism that provides a resource when an environmental challenge resembles historical conditions.”

The ammonite and chicken examples differ in their evolutionary extent, one being truly evolutionary in terms of time and biology, the other an example, over a much shorter term, of individual adaptations. Though the two examples almost certainly differ in the detail of their genetic and molecular basis, the bird example demonstrates atavism mechanistically, and illustrates molecular processes that may resemble those that contributed to atavism in ammonites.

Thus, innate, possibly dormant, processes can be a resource for biological response to environmental challenge. This is inconsistent with the widely held view of an evolutionary mechanism in which evolution depends solely on adaptations being generated by a random process. As suggested earlier, a process in which biological solutions are generated at random seems unlikely to have led to atavism repeatedly being the solution to the extreme environmental conditions that caused mass extinctions of ammonites. The implication is that organisms faced with changing environmental conditions can depend on more than chancy randomness; other phenomena might supplement random mutation in the generation of variation, perhaps in ways that enhance the generation of variations that match environmental opportunity or threat. There are, in fact, ways in which organisms generate adaptation through direct and specific reaction to changes in their environment.

Plastic butterflies

The squinting bush butterfly (Bicyclus anynana) is found in tropical woodland in east Africa7. Like many butterfly species, they have spots on their wings. Some of the spots look like eyes, and are likely to be a defensive feature. Others, on less visible parts of the wings, are used in signalling between sexes during courtship. The spots aren’t a permanent feature, they exhibit seasonal change. The tropical regions where these insects live have distinct dry and wet seasons. In the latter the exposed eye spots are large and very visible, whereas in the dry they are much smaller and less distinct. These alternate phenotypes (morphs) probably correspond to the degree of threat from different predators in the two seasons. In the wet season, the threat comes predominantly from invertebrates such as mantids, and large eye spots are likely to threaten or distract this type of predator. This changes during the dry season when birds become the main predator; shrinkage and fading of the spots reduces the threat from birds by making the butterflies less visible.


The squinting bush butterfly – dry season morph (left), wet season morph (right).

Image credits:
Left; Brian du Preez, https://uk.inaturalist.org/photos/15229584?
https://www.facebook.com/brian.botanist/

Right; Robert Taylor, https://uk.inaturalist.org/photos/116808542?
https://uk.inaturalist.org/people/robert_taylor

Individual butterflies do not alternate between the two morphs; their adult lives take place within one or other of the two seasons, and they are committed to the one, corresponding morph. This one species therefore has two adult phenotypes, depending on the environmental conditions into which the adult phase is hatched, a phenomenon known as plasticity. Plasticity may be defined as the ability of a single genome to generate different phenotypes in response to varying environments. In other words, an organism’s genes may not necessarily code for a single overall phenotype, instead, they may enable organisms’ phenotypes to be flexible and environment-responsive.

Plasticity extends the range of environmental conditions that the squinting bush butterfly can tolerate as adults (not all butterfly species can tolerate different seasons and they often spend harsh ones as pupae, or migrate thousands of miles as in monarch butterflies). Similar seasonal plasticity is seen in other organisms, such as changes between summer and winter plumage in birds or fur in mammals. In all these cases the environmental changes to which the plasticities are linked are repeated and quite predictable, thus the plastic responses to them are consequently distinct and very specific. In other words, these plasticities are responses to normal environmental changes anticipated within the animals’ biology. But plasticity also enables phenotypic adjustments to unexpected environmental circumstances.

Ready to use adaptation in a frog

The wood frog (Lithobates sylvaticus) is found throughout much of Canada, Alaska and the mid and eastern United States, living in wet woodlands that are swampy or have ponds. The extent of agriculture in North America results in woods being frequently close to farmed land, and these frogs consequently being exposed to pesticides. Research has shown that phenotypic plasticity provides them with a way to tolerate pesticide exposure, and is also generating permanent changes in this animal’s populations8.

Image credit: Jomegat, CC BY-SA 3.0 https://creativecommons.org/licenses/by-sa/3.0, via Wikimedia Commons
https://jomegat.wordpress.com/

Carbaryl is a synthetic insecticide widely used in agriculture and horticulture. Woodland ponds may become exposed to Carbaryl as run-off from agricultural land, and it is toxic to aquatic animals including fish and amphibians. Clearly, ponds closer to agricultural land often have higher concentrations of Carbaryl pollution than those further away, so exposure of frogs to the insecticide is closely related to agricultural proximity. That in turn correlates with how sensitive the frogs are to its toxic effects. When tadpoles are exposed to Carbaryl in the laboratory, those from ponds close to agriculture are less sensitive to it (measured as the proportion of tadpoles that survive a known toxic dose) than those from ponds further away. (The distances from agriculture of ponds from which frog eggs were taken ranged from a few metres to about half a kilometre.) Being from sites with greater insecticide exposure therefore seems to have given tadpoles extra resistance to Carbaryl. The story becomes more interesting, though, when the question is raised as from where that resistance comes. Because it’s not that the tadpoles from agriculture-distant ponds don’t have Carbaryl resistance, only that it isn’t activated. If tadpoles are exposed to a low, non-lethal dose of Carbaryl for a period prior to being exposed to the toxic dose, the agriculture-distant ones become resistant to it. Pre-exposure of tadpoles from agriculture-proximate sites makes little difference to their degree of Carbaryl resistance. What this shows is that the ancestral condition of wood frogs (represented by those tadpoles from sites with little or no Carbaryl pollution) is that they have resistance that can be induced, whereas frogs from populations with experience of insecticide exposure have resistance that is permanently expressed (the term for which is constitutive).

Continued and biologically significant exposure to insecticide has caused a change in important biological processes within these frogs. The change to constitutive expression of resistance benefits them because they are in an environment where lethal pollution may be constant or frequent. Since they do not encounter resistance-inducing, low concentrations of pollutant, constant resistance to toxic concentrations is needed instead. These frogs have adapted to this severe environment and, importantly, that adaptation is innate, a genetic trait with which subsequent generations are born. Plasticity has therefore been the starting point for a change in the biology of these pollution-exposed frogs. A phenotypic variation in the form of a variable resistance has provided an advantage on which natural selection has been able to act, yielding a new, fixed and heritable phenotype which has better fitness in the altered, more adverse environment. (The experiment was carefully designed to discriminate between this mechanism and other ways in which the heritable resistance could potentially have occured.)

” … a variable resistance has provided an advantage on which natural selection has been able to act, yielding a new, fixed and heritable phenotype which has better fitness in the altered, more adverse environment.”

That heritable fixation is termed assimilation9. It is not yet fully clear how assimilation takes place, but well established, related laboratory research has shown that it can be dependent on natural selection acting upon animals with altered plastic characteristics. It may be that processes activated by stress (in this case the toxic effect of the pollutant) are involved. There is evidence to suggest that animals carry genetic mutations whose effects are usually suppressed, but can be released by stress induced processes. These are called cryptic mutations, and certain of them might act to change inducible genes into constitutive ones10 11 12 13. Alternatively, a similar genetic change from inducible to constitutive phenotype might also be the result of stress increasing the rate of genetic mutation14.

Ready to use adaptation in a snake

Plasticity affects a range of biological phenomena including behaviour, ecological interactions and morphology. An example of the last is that of plasticity in the head size of tiger snakes (Notechis scutatus)15.

Tiger snakes live in southern and central Australia and are venomous carnivores that prey on small vertebrates such as frogs, birds and mice. In addition to their ancestral populations on the Australian mainland, there are several populations on islands. Some of these were established thousands of years ago when sea levels were lower, enabling migration to take place, others much more recently (less than 100 years ago) through human activity. It happens that their prey animals tend to be larger on the islands than on the mainland, to an extent that makes them more difficult to capture and swallow. Once again, plasticity and subsequent assimilation are how these animals adapt to this problem.

Image credit: David Cook Wildlife Photography
https://www.flickr.com/people/kookr/
https://uk.inaturalist.org/photos/51890

Generally, island snakes are bigger than their relatives on the mainland, and this includes having larger heads. Experiments show that head size in snakes from recently colonised island populations is plastic in that snakes fed on larger mice develop larger heads than those fed on smaller ones. However, that plasticity is not seen in snakes from islands colonised several thousands of years ago; these snakes have a large head phenotype regardless of the size of mice they are continually fed on in experiments. The long established island tiger snake populations therefore appear to have large heads by default, i.e. they have assimilated large head phenotypes of a formerly plastic head size range.

Having shown adaptation arising from plasticity in wood frogs and tiger snakes, we now go on to discuss plasticity’s relevance to evolution, and how this contrasts with the traditional view.

Plasticity is a source of variation

”Plasticity resists the threatening effects of dangerous changes to environments in two ways.”

Phenotypic plasticity and assimilation therefore enable small but beneficial changes when animals face environmental stress. In the above examples the animals  remain wood frogs or tiger snakes, but are adapted variants of their recent ancestral population. In other words, in a small, incremental way, they have evolved.  Plasticity resists the threatening effects of dangerous changes to environments in two ways. First, where environments are unstable, it is a mechanism of continuous adjustment to environmental fluctuation. Second, when environmental change is more severe and / or permanent, plasticity can act via assimilation as the basis for a mechanism of permanent, genetically innate adaptation, which may contribute in the longer term to the emergence of new species.

By its nature, plasticity is a special form of phenotypic variation, deployed as pliable traits responsive to environmental change. In the wood frog and tiger snake examples, since the permanent adaptations take the form of now fixed points on previously variable ranges in characteristics, the plasticity has acted as the source of variation on which natural selection has acted. The adaptations we have described (a biochemical one in wood frogs, a morphological one in tiger snakes) have therefore not originated from random genetic changes, rather, they began with organisms exhibiting specific forms or extent of plastic traits (the enabling phenotypes) that had greater fitness in changed environments. Plasticity therefore channels biological responses to environmental change in specific, narrow directions. Then, if the altered environment is maintained (the consequences to the animals, though moderated by the plastic response, still being significant)  additional variations may cause assimilation. In some cases these variants may complement the enabling phenotype (e.g. by giving it constitutive expression or tuning it in other ways), and continuing natural selection will cause these to spread through and dominate the population.

”These adaptations have not originated from random genetic changes.”

”The involvement of genetic change has been led by this plasticity-enabled process.”

This route to adaptation and evolution certainly involves mutation, but the contribution mutation makes is highly dependent on the nature of the plasticity. The adaptive approach to the environmental challenge has been enabled by variation present in the form of the plasticity. The involvement of subsequent genetic change has been led by this plasticity-enabled process, and has caused permanence or enhancement of the adaptation. This influencing of adaptive direction by plasticity has a powerful, indeed profound consequence: adaptive solutions to threatening environmental change are frequently not random in their origin or, consequently, their nature. Rather, plasticity directs them, guiding the adaptive mechanisms specifically to the nature of the stress. Instead of responses to environmental problems having to emerge from chance events, plasticity offers existing phenotypes that are already applicable.

Adaptations are the basis of evolution. A single fitness-improving change in a biological trait will not usually cause the animal’s species to change; new species arise when combinations of changed characteristics make an animal population significantly and permanently distinct from its ancestors. The island populations of those tiger snakes that migrated thousands of years ago, and which have a permanently large rather than plastic head size, have adapted but not changed to an extent that they are now new subspecies. If new environmental challenges appear, perhaps the resulting additional adaptations will cumulatively cause them to speciate. The few thousands of years since their first island occupation is a very short time on the evolutionary scale and, currently, they remain merely a variant within the species Notechis scutatus.  It is, however, possible to see examples in which plasticity has played a distinctive role in the emergence of a new species.

”It is possible to see examples in which plasticity has played a distinctive role in the emergence of a new species.”

Evolution of an athlete

Tibetan antelopes (Panthelops hodgsonii) live at high altitude on the Tibetan plateau. They have outstanding physical capability at altitudes (up to 5,500m) that, for most mammals, is extreme and very strenuous, if not impossible, to survive.

Image Credit: Marc Faucher

https://uk.inaturalist.org/photos/27823297?size=medium
https://mrfaucher.blogspot.com/
https://creativecommons.org/licenses/by-nc/4.0/

One way animals resolve problems relating to oxygen supply is by using different forms of haemoglobin, the oxygen transport protein in red blood cells. In mammals it takes the form of an assembly of four protein molecules called globins, and there are different globins that can be included in that four-component structure. For example, most mammals have foetal and adult specific globins, which differ in how strongly they attract and bind oxygen (i.e. their affinity for oxygen). Haemoglobin in adults partly comprises adult specific globin (there are others as well but, for clarity, this is detail we can ignore without compromising the point we’re describing). But in foetal blood adult globin is wholly or partially replaced with a foetal one, forming haemoglobin molecules that, having higher oxygen affinity, contributes to the difficult and critical process of transferring sufficient oxygen across the placenta, to the foetus.


”Sheep and goats also have another use for this third globin, in a plastic response to hypoxia.”

Sheep and goats have a third form of haemoglobin, one partly composed of a globin that is present in lambs and kids. This juvenile globin also has a comparatively high oxygen affinity and additional blood oxygen may help infant animals at a stage when they remain very delicate. Sheep and goats also have another use for this third globin, in a plastic response to hypoxia. When adults are subjected to low oxygen concentrations they change their haemoglobin constituents, reducing the proportion of adult globin and replacing it with the juvenile one. The physiological benefit of this is obvious. Molecular biological studies have shown that this ability to switch from adult to juvenile globin use when oxygen is decreased, have been inherited from a common ancestor of sheep and goats.

Tibetan antelopes share that ancestor, and they have adapted to extremely high altitude by further refinement of these globins16. First, a deletion of their DNA has resulted in the adult globin being lost; these antelopes do not have the gene for it. Second, that lost globin has been functionally replaced by the formerly juvenile one, which is no longer plastic, but expressed constitutively in adults. A critical aspect of the evolution of these highly specialised animals, then, has been the redeployment and assimilation of a formerly plastic response to altitude possessed by an ancestor (and still present in sheep and goats), resulting in the default use of a high oxygen affinity form of haemoglobin much more suited to the difficult environment these animals now endure.

”A critical aspect of the evolution of these highly specialised animals has been the redeployment of a formerly plastic response to altitude possessed by an ancestor.”

Their being athletic at altitude is central to the ecological strategy of Tibetan antelopes; it is how they exploit their extremely high altitude home. Athletic capability in a hypoxic environment almost certainly requires greater physiological capacity than sheep and goats have, and constant rather than inducible expression and deployment of the juvenile haemoglobin is likely to contribute to that. That the constitutive condition probably evolved from an inducible one in ancestor of the antelopes is logical because of the plasticity’s clear role in evolution of altitude tolerance as shown by its importance to the sheep and goats (the research paper describes, with evidence, the evolutionary sequence of this animal group). Furthermore the plasticity is likely to have contributed to the assimilation events in which genetic change (in this case a deletion) led to permanence of a position in the former range of juvenile haemoglobin expression levels the plasticity involved. This is because natural selection is essential for such genetic changes to spread and eventually establish new, adapted populations. In this case, the selecting environmental factor would partly have been the high altitudes the ancestors were already encountering enabled by their plasticity. There would therefore have been a mechanistic link between the plasticity in juvenile haemoglobin expression and its own genetic assimilation in the form of permanent expression.

Clearly, there is far more to the identity of Tibetan antelopes than this single evolutionary adaptation. However, it is distinctive and critical to this species; without it, these animals would not have secured the advantage of being able to survive in an environment with few or no resource competitors and one that is difficult for predators. Their evolution has involved many and diverse adaptive changes, but that redeployment of a plastic response to altitude change was a formative event and beautifully illustrates plasticity as an innate resource for adaptation and how this can instigate the formation of new species.

Transmitting parental experience

The power of plasticity as a process of adaptation and evolution is very much a consequence of the way in which it provides phenotypic variation that, rather than being random, is directly related to the nature of environmental challenges. In doing so plasticity reduces the immediate effect of changes in environmental conditions (be they competition, habitat loss, food availability, predation, altitude, etc.), adjusting phenotypes to positions on their ranges that are adaptive. In the longer term, if the environmental condition is maintained, natural selection may act permanently to shift to this adaptive position. Plasticity, then, 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 random mutation based concept of adaptation.

Crude oil pollution is dangerous to most organisms and their habitats partly because of its viscous nature (as in major accidental spills) and partly because of the large number of toxic chemicals it contains. Fish are among the organisms exposed to oil pollution and its poisonous effects, which often involve interference with embryonic development resulting in reduced hatching and hatchling survival, morphological deformation, biochemical and neurological alteration, and behavioural change. These effects are of interest to scientists because of their ecological importance and the insight they can provide to cellular and developmental processes. Zebrafish (Danio rerio) are frequently used for laboratory studies in this area of environmental science. 

In the study in question17, adult zebrafish (Danio rerio) were exposed in their diet to an extract of crude oil containing many of the chemicals known to cause the oil’s toxicity. After a period of this treatment the fish were mated and progeny larvae also subjected to oil exposure. Both the parent adults and the larvae were subjected to a range of tests for any effects of the oil on their tissues and health. Oil treatment had no effects on the morphology or general health of the adult parental fish, though their fertility was reduced. Larval progeny are known to be particularly sensitive to chemical pollutant exposure, and this was confirmed by comparing the effect of oil on progeny from untreated parents; they had reduced survival compared with an untreated cohort.

However, larval progeny of oil treated adults were partially resistant to this oil toxicity; survival of populations of these larvae was 30% greater than oil treated larvae from parents that had not been exposed to oil. The extent of phenotype change in the progeny from oil treated parents became even more apparent with the observation that their survival decreased when they were raised in clean water with no oil exposure. These larvae are therefore phenotypically adjusted to the oil contaminated environment. The striking aspect of these results is that the phenotypes of the progeny larvae is dependent on the experience of their parents; even though parent fish have been minimally affected by oil, their treatment has promoted a change in their offspring. This is an unexpected observation because though something passed from the parents is causing the phenotype change (i.e. it has been inherited), that heredity cannot have occurred through a genetic mechanism (the rates at which genetic mutation and other genetic changes occur mean that it is impossible that the toxicity resistance arose in this way in such a high proportion of affected larva). Instead, this transgenerational transfer of toxicity resistance appears to be an ‘epigenetic’ effect, i.e. a heritable change in gene function that has occurred without a change in the DNA sequence.

”Larval progeny of oil treated adults were partially resistant to this oil toxicity”


”That heredity cannot have occurred through a genetic mechanism”

”Chemical marking of genes in these ways enable gene expression patterns, and hence phenotypic traits that are variable, to be transferred from one generation to another.”

Over a century of genetic science established and increasingly supported a heredity mechanism based entirely on the code contained in organisms’ DNA. That view has altered substantially in recent years not least because advances in research techniques have revealed how additional features of genetic material influence how genes behave. It is beyond question that DNA is the principal transgenerational carrier of hereditary information in the form of the genes that it encodes. Biota and cells are their phenotypes, and phenotypes are the combined result of the genes carried by organisms and the patterns in which they are expressed.  It follows that if specific combinations of expressed genes can be maintained between generations then that provides another contributor to heredity, one that potentially introduces the influence of parental condition and experience to it.

That argument was long countered by the fact that during animal reproduction adult patterns of gene expression appear to be stopped. However, recent research into how other molecules initiate or repress gene function by physically and chemically interacting with DNA has revealed that there are notable exceptions to this resetting of gene expression. Two types of such interaction are of interest here. These are methylation, the addition or removal of small chemical groups to DNA nucleotides, (the four components whose sequences comprise its coded information), and the addition or removal of chemical groups to histone proteins, which are important components of the complex structures in which DNA is mounted and that are important in the mechanisms of gene function. The chemical marking of genes in these ways enable gene expression patterns, and hence phenotypic traits that are variable, to be transferred from one generation to another. (There is a further biomolecular entity that causes epigenetic effects which will be discussed later.)

See a summary diagram of epigenetic marking.

Guinea pigs and the biology of climate change

A recent study related to climate change illustrates inducible epigenetic marking and its inheritance18. This study examined the responses of wild guinea pigs (Cavia aperea) to heat. The same males were twice mated to the same females; once before and once after a two month period in which the males were kept at an unusually high temperature (30°C as opposed to normal temperature of about 20°C). Examination of DNA in liver biopsies taken before and after the heat treatment (the liver is important in temperature control in mammals) showed widespread differences of parts of the DNA molecules that had attached methyl groups. Not only that, but such differences (called differentially methylated regions, or DMRs) were also found between male progeny generated from the matings that took place before and after parental heat exposure. This indicates first that the fathers’ liver function changed in response to their heat experience, and that those changes involved altered patterns of DNA methylation and consequently patterns of gene function. Second, it shows that the sons inherited their DNA methylation patterns from their fathers (whether they were fathered before parental heat treatment or after it). In fact, it appeared that heat treated fathers passed on some DMRs that were identical to their own and some that weren’t, suggesting that these fathers passed on biological changes additional to those they themselves had in their livers. DMRs associated with the parental heat treatment were present in both liver and testes of the progeny, the latter indicating the possibility that they could be passed to subsequent generations, though that  was not tested. The genes encountering changes to their methylation included some known to be involved in stress responses and temperature regulation, as well as regulatory genes that take part in wider cellular and developmental processes.

The environmentally induced responses to demanding conditions by zebrafish and guinea pigs demonstrate heritable phenotypic alteration that is not caused by genetic variation (i.e. variation in the genetic code) but by epigenetic change to the DNA’s chemical structure. In these epigenetic processes we therefore see two levels at which phenotypic plasticity provides adaptation to environmental change that differs from the conventional model in which random mutation generates phenotypic variation that is acted upon by natural selection. At phenotypic level, inducible plasticity is a source of variation, one that provides variation directly related to the nature of the inducing environmental stress. At the molecular level, rather than inducing random changes to gene structure, plasticity’s mechanism involves chemical marking of DNA that occurs directly and specifically in response to environmental change and that can be heritable. This is a process that enables immediate responses to environmental change and threat, responses that match the changes, and that can be passed on transgenerationally to adapt progeny against a continuing threat.

The study’s lead author, Dr Alexandra Weyrich, is also one of the authors of this science comic book on epigenetics.

These laboratory studies strongly suggest that epigenetics can enable adaptation to problematic environments, in these cases pollution and an aspect of climate change. There is also good evidence, described in the next section, that it does so in real situations in the wild.

Epigenetics and environmental adaptation in the wild

The New Zealand fresh water mud snail (Potamopyrgus antipodarum) was inadvertently introduced to the United States probably in the mid 1980s and has become seriously invasive. Though its occupation of the new habitats is very recent in evolutionary terms, alterations are already appearing in its phenotype. The rapidity of its occupation and phenotypic change make this a useful animal with which to study adaptation. The shapes and colouration of their coiled shells are important distinguishing features of different snail species. However, individual species have long been known to exhibit variation in their shell shapes, often in response to the forces of water (e.g. river flow or wave action) to which they are exposed, and a study published in 2017 showed that this is the case with the New Zealand snail19.  

Image credit: United States Geological Survey
https://commons.wikimedia.org/wiki/File:P_antipodarum.jpg

Examination of these snails in lakes and rivers in the northwestern US showed that the size of the apertures at the bottom of their shells (measured as the ratio of aperture diameter to shell height) correlates with the speed of habitat currents. Shell apertures in snails living in a fast flowing river were larger than those of snails in a slower one, and still smaller in snails located in lakes that have no appreciable flow. This is an adaptive correlation; the larger aperture accommodates a larger foot, which gives the snails better grip in fast currents, making them more effective in their grazing on the micro plant and sedimentary material they eat. Importantly, these habitat associated phenotype variations have emerged since the occupation of the US habitats; they have not come from existing variants among invading snails from New Zealand. (In fact, all the populations studied are clonal; by a particular feature of the species’ reproduction process, a large proportion of populations of it now present in the US, including the four included in the study, are derived from a single invading female.)

Phenotypic variation in these snails has therefore enabled them to occupy niche habitats as part of their progressive invasion of a new continent. Additionally, a special biological feature of New Zealand mud snails makes the occurrence of that variation intriguing. This animal has the capability to reproduce asexually. In this process, females possess progeny embryos at birth, and the progeny are clones, genetically identical to that female parent. This asexual process has an important impact: progeny lack the genetic variation that results from the shuffling effect of sexual reproduction. As already mentioned, the four snail populations used in the study (and indeed others across the western US) are derived from a single invading female. This means that there is virtually no variation between the DNA of snails in these populations because they started as identical clones and the few decades since their clonal origin is far too short a time for many mutations to arise amongst them. So if snails at the four different habitats are genetically identical, how can they differ in their phenotypes? Indeed, the scale and rapidity of their invasion suggest that the species is very adaptable; if there is no genetic variation then there must be an alternative mechanism for that phenotypic versatility. The study went on to reveal a further correlation with the different habitat water flow rates, this time a molecular one. Specifically, the DNA of snails at the different habitats differ in their methylation, their methylation patterns being very specific for the lake and river habitats. Therefore, whereas the coding sequences of the DNA molecules are identical in these snails, their DNA methylation is not, and consequently the different snail populations almost certainly have different patterns in the activity of many of their genes. Epigenetic chemical marking of DNA therefore provides a potential source of phenotypic variation in these animals. The investigators acknowledged that at this stage they have not yet fully proved that the epigenetic changes are the cause of the shell phenotype alterations, but it is likely that they are. There is also reason to believe that the different patterns of gene marking have been induced by the different environments of the snails’ habitats.

”If snails at the four different habitats are genetically identical, how can they differ in their phenotypes? Indeed, the scale and rapidity of their invasion suggest that the species is very adaptable; if there is no genetic variation then there must be an alternative mechanism for that phenotypic versatility”

This example calls into question, in two ways, the exclusivity of random gene mutation as the source of phenotypic variation in adaptive evolution. First, it shows very rapid adaptation in an animal that simply does not have genetic variation. Second, it supports the idea that epigenetic processes can enable phenotypic variation, and consequently adaptation, in wild populations (rather than merely in laboratory situations). Additionally, there is another type of epigenetic inheritance that differs even further from the classical genetics mechanism.

Confronting a tenet of biology

The biology of wound healing might seem a dry subject, underwhelming to all but a specialist. But research into possible epigenetic effects in wound healing has revealed an aspect of it that is profound. The way wounds heal changes with ageing. Embryos can heal their wounds without leaving scars, but that is generally not the case in adult animals, and scarring plays a role in the progressive declining health associated with age. In other words, although scarring is a mechanism of wound healing, it can itself cause continuing medical problems (e.g. the scarring in lungs caused by pneumonia and silicosis). Livers have a notable ability to recover from wounding; they can regenerate after substantial loss or damage of tissue. This reflects the importance of liver in dealing with toxicity; it has to be good at recovering from damage itself (e.g. from toxic chemicals) if it is to provide protection for the rest of the body. The recovery from some types of liver damage does leave scarring, but the process can be plastic.

Experiments have shown that the progeny of male rats that have been exposed to a liver damaging chemical have substantially less liver scarring than their parent when exposed to the chemical themselves20. So the environmentally challenged male parents seem to have changed the wound healing response in their progeny (the effect was passed on through at least two generations). The problematic effects of scarring suggests that this transgenerational resistance to it may be an adaptation, endowing improved fitness on the progeny. Given what we have already shown in preceding examples of epigenesis, perhaps this isn’t altogether surprising. However, a clue suggesting something particularly special in this effect is that it seems restricted to liver; ancestral liver damage does not reduce chemical scarring that occurs in kidneys of toxin treated progeny. This, and other experimental evidence indicated that the environmentally induced transgenerational anti-scarring effect is highly specific to liver rather than being a general one affecting other organs. Such specificity raises a logical problem: if this process is so specific to liver, excluding other organs, how can it be transgenerational if the testes, and consequently sperm (the toxin exposed parents in these experiments were the fathers), are excluded from it? That question led the research group involved to test for a possibility that had long been considered impossible: transfer of genetic information from somatic tissue to the germ line.

Researchers took blood serum from male rats treated with toxin exactly as in the earlier experiments, having allowed a period for the animals to clear the toxin from their systems, and transfused it into other untreated male rats. They found that this exposure to the serum of toxin-exposed rats generated epigenetic changes, in the recipient rats’ sperm, to genes known to be directly involved in the scarring process. (Specifically, scarring involves a process of differentiation of a type of liver cell, stellate cells, that change into a new type called myofibroblasts; these genes are highly important in the control of that differentiation process.) The observed changes to the chromatin of these genes are very likely to alter their expression in a way that could inhibit the scarring process. So the serum recipient rats’ sperm have undergone an epigenetic change likely to make them capable of passing on an anti-scarring capability to their own progeny, even though they themselves were not exposed to the toxin.

This suggests that toxin treatment of male rats results in something being secreted into blood that carries a signal to their testes, causing epigenetic changes to genes that control aspects of liver phenotype. In this way the rats’ adult bodies have apparently conveyed an instruction to their sperm and hence to the next generation. The researchers conducted further experiments that established that the signal molecule comes from the affected organ, the liver, and specifically from the stellate cells. It appears, therefore, that an acquired alteration in the phenotype of an organ is causing changes to the hereditary material of these animals (their germline) that makes the acquired trait heritable.

”This suggests that toxin treatment of male rats results in something being secreted into blood that carries a signal to their testes … ”

This is very disruptive. Animals have a separation between the cells responsible for reproduction (the germline) and those that form the embryonically developing and adult body and organs (the somatic cells, or soma). A classic, central tenet of genetics, that, in animals, hereditary information can flow in one direction only (the “Weismann barrier”21), from the germline to the soma, has been questioned by this research. The idea of information passing in the reverse direction, from soma to germline, i.e. that the soma can change its phenotype and make those changes heritable by inducing changes in the germline, has long been considered impossible, largely because of huge difficulty to date in conceiving a biological mechanism. This experiment is highly persuasive of an inherited trait arising in a soma to germline direction, and suggests where to look for a mechanism: some kind of an information carrier transported by blood.

Messages from changing phenotypes

Advances in biology are often the result of discovery of important new molecules; this is partly why the field of molecular biology has come to dominate biological and medical research. In the mid 1990s some puzzling results from genetics research led to the discovery of a new class of molecules; previously unknown forms of ribonucleic acid (RNA) found in sperm. For more than half a century RNA has been known as a principal part of the cellular mechanism through which genes work by producing proteins. RNA is a polymer very similar to DNA, but differs in a subtle chemical way that results in its having quite different structures. Importantly, it can occur in a variety of two and three dimensional forms. Three of these form key components of protein production machinery: messenger RNA that carries coded information about a protein’s sequential chemical structure from the gene to the cell’s protein assembly site; ribosomal RNA that forms a kind of jig on which the assembly takes place; and transfer RNA which is an adaptor that translates genetic code and uses that information to direct the assembly of strings of the amino acid molecules which constitute proteins.

Image credit: Rfam database, Public domain, via Wikimedia Commons
https://upload.wikimedia.org/wikipedia/commons/0/0c/BsrC_secondary_structure.jpg

What happened in the 1990s was the surprising discovery that biologically important forms of RNA molecules are not limited to these three, but also include a set of molecular types generally called non-coding RNA (ncRNA). (Transfer RNA and ribosomal RNA are non-coding RNA molecules so, strictly speaking, these recently discovered molecules have extended an existing classification of RNA.) Amongst ncRNAs are several involved in the control of many cellular processes, mainly via participation in gene expression control (note that they were discovered in sperm, but are also found and are operational elsewhere). Some characteristics of ncRNAs are of particular interest in the context of adaptation. First, their location in sperm extends the nature and amount of information that sperm can carry from one generation to the next. Second, ncRNAs carry information and instructions between different cells and tissues. They do this by being mobile, travelling between different locations in animal bodies in blood and other body fluids. That mobility often involves small carrier structures called extracellular vesicles, and in some cases ncRNAs being transported as molecules dissolved in body fluid. These characteristics enable an epigenetic process that may prove to be an important route through which environmental conditions can influence evolution.

Extracellular vesicles and ncRNAs, then, are intercellular communication agents; they carry epigenetic information between different cells, and that, of course, is the very characteristic sought in identifying the blood soluble factor acting as the messenger in the liver wounding example. To date, there is no report demonstrating that extracellular vesicles and ncRNAs are the agents that act in this particular case,  but other lines of research strongly suggest that they do transfer epigenetically heritable information from soma to germline. For example, in one study22, human tumour cells were grafted into mice. Those tumour cells had been modified to carry a gene foreign to both humans and mice, in order to make the tumour cells produce an RNA that would not normally be present in the mice and was easy to detect experimentally. Experiments showed that the tumour cells released extracellular vesicles containing the foreign RNA into the mice’s blood. Furthermore, the foreign RNA was also found in the mice’s sperm. (The researchers went to great lengths to ensure that the foreign RNA they detected was not present as the result of contamination or other trivial events.) These experiments are impressive and persuasive. The clever experimental design has demonstrated quite securely the transfer of RNA from soma to sperm because in this case the soma was the only possible source of the foreign RNAs; they simply could not have come from anywhere else.

Image credit: Charles Darwin, Public domain, via Wikimedia Commons
https://upload.wikimedia.org/wikipedia/commons/c/c1/Darwin_Variation_1868_title_page.jpg

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.

In his 1869 book ‘The Variation of Animals and Plants Under Domestication‘ Darwin suggested the possibility of particles present throughout the body that are continuously transferred to gonads, carrying heritable information. Among other biological phenomena, he surmised these ‘gemmules’ as a mechanism through which the body (i.e. the soma) could react to environmental conditions with the resulting change becoming hereditary. The soma to germline information transfer mediated by ncRNA and extracellular vesicles is remarkably close to that theoretical mechanism developed by Darwin s century and a half ago.

Non-coding RNA and inherited experience

A striking example of epigenetic adaptation first reported in 2014 has recently been shown to involve ncRNA22. This work was based on an experimental system in which mice are conditioned to associate an odour with an irritation, a mild electric shock. Short periods of repeated delivery of a distinctive chemical smell followed by a shock resulted in the mice exhibiting anxiety when they smell the odour, even when no shock is administered. The conditioning was very specific for the actual odours being used, rather than exposure to odours in general; mice conditioned with one odour did not become anxious when exposed to another. This experimental system enabled a test of whether such environmentally induced behavioural changes can be inherited. The result was positive; when, subsequent to the conditioning process, conditioned mice were mated, two generations of progeny exhibited the same anxiety response to specific odour seen in their parents.

Not only that, but the inherited phenotype involved morphological changes to odour detection organs. Odour detection involves tissues in the nose and brain that have channels specific for different types of odour. The number and size of anatomical structures comprising the olfactory channel known to detect the conditioning odour used were increased in the affected progeny. The conditioned mice therefore pass to their offspring a state of preparedness for an environmental condition they have encountered. That preparedness comprises two linked but separate phenotypic components: the sensory one and the neurological one controlling and enabling the behavioural (i.e. the anxiety) response.

These observations show that animals can inherit altered behaviour when their recent ancestors experience adverse environmental conditions. It is easy to see that such transgenerationally transmitted behavioural change could be beneficial, increasing survival prospects when there is environmental threat. This research has therefore shown that environmentally induced behavioural change may have evolutionary potential. (It may also hold clues to the biological origins of instinct.)

”This environmentally induced behavioural change is therefore transmitted transgenerationally by RNA in sperm of affected mice.”

The same research group has recently followed up their demonstration of this adaptive epigenetic process with experiments indicating that it has an RNA based mechanism23. They did this by extracting RNA from sperm obtained from conditioned male mice then injecting it into single cell embryos taken from unconditioned females that had been mated with unconditioned males. The only link of these embryos to conditioning was therefore the RNA with which they had been injected, but that was enough; when they became adult the injected embryos showed the odour linked anxiety response and the morphological enhancement of odour detection organs observed previously in progeny of conditioned parents.

This environmentally induced behavioural change is therefore transmitted transgenerationally by RNA in sperm of affected mice. (Note that there is reason to think that this mechanism may not be the only one, but the possibility of other epigenetic mechanisms doesn’t affect the argument.) The research group has not, to date, shown how this phenotype transforming RNA comes to be in the sperm, but it may well have arisen in the somatic tissues (the odour detection organs and brain networks) that provide the conditioned response. The transfer of functional information from cell to cell and organ to organ is what non-coding RNAs do, and other research has shown them to be present in sperm and to generate biological effects in animals sired by those sperms. This, therefore, may well prove to be an example of adaptive change generated by a soma to germline epigenetic process in direct response to environmental conditions.

Research on this epigenetic process is at an early stage and much still remains to be discovered before the phenomenon is fully understood. Nevertheless, these three examples (the experiments involving liver wounding, tumour cell grafts and odour associated anxiety) collectively show how somatic cells with environmentally induced changes to their phenotypes send information to germ cells, thereby making the new phenotype hereditary. 

”These three examples … show how somatic cells with environmentally induced changes to their phenotypes send information to germ cells making new phenotypes hereditary”

The theory of a barrier that restricts information flow and influence to a germline to soma direction, thereby preventing phenotypes from specifying heredity21, has been a barrier to thinking about the interaction between environments and animal evolution. The demonstration of hereditary information passing from somatic cells to germ cells and thence to progeny seriously weakens that theoretical barrier. In doing so it allows a potentially powerful way in which animals can adapt reactively and specifically, rather than only randomly, to environmental difficulty and opportunity.

Culture as a tool of evolution

Clearly, for a mechanism of phenotypic variation to contribute to evolution it must be hereditary; that is why so much of evolutionary biology concerns genetic science and molecular biology. However, not all heredity is genetic, there is an alternative form of heritable variation which can be seen in a species that is reputed to be the most widely distributed mammal in the world, after humans24.

Killer whales (Orcinus orca) are highly social animals: they live in familial groups, have complex patterns of vocal communication, and coordinate some of their activities including cooperative hunting. There are several types of killer whales, differing in their morphology (body markings, appendage shape and size), in the marine areas and habitats they prefer, and the animals they prey upon (fish, marine mammals and birds). Importantly, these animals have culture: complex behaviour that is specific to individual social groups and passed on between and within generations through social learning. Socially maintained behaviour includes food preference, for example rigidly exclusive diets of either fish or marine mammals that are distinctive characteristics of some killer whale types, together with the techniques used to hunt them. The complex sounds used for hunting, navigation and communication, are also distinctive for different groups (including dialects specific to individual killer whale pods and clans) and are probably socially learned24 25.

Image credit:
Viki Kolatkova
https://uk.inaturalist.org/photos/92291143

Killer whale behaviour (e.g. different hunting methods associated with individual groups’ preferred prey) probably reflects their intelligence. Intelligent social animals such as apes and dolphins (killer whales are part of the oceanic dolphin family) are known to experiment and develop complex behaviours such as tool-use26. Killer whales, then, are likely to develop new behaviour through innovation25. This ability to develop successful new behaviour and for it to spread and be maintained in animal groups by cultural learning is a strongly adaptive capability, enabling animals to improve their activities and react behaviourally to environmental changes, be they threats or opportunities. Maintenance of behaviour through successive generations through cultural learning is a non-genetic form of heredity.

”Maintenance of behaviour through successive generations through cultural learning is a non-genetic form of heredity”

”Gene-culture interactions mean that culture in animals is an evolutionary mechanism”

Another important aspect of culturally maintained behaviour is that, being adaptive, it affects fitness. Consequently, Killer Whale familial groups that have successful variations in behaviour can have selective advantage over other groups. The resulting increased success of the former group might therefore lead to it expanding and increasing as a proportion of a wider orca population, a case of natural selection acting on a non-genetic, behavioural variation. Should that occur, other phenotypic variations in the behaviourally favoured familial group (which, for example, might be morphological such as differences in body markings or appendage shape, or biochemical such as altered digestive enzymes) will follow selection of the behavioural variation; their presence in the wider population will increase as the group expands. Such phenotypic variations will, of course, be genetically encoded, which means that a culturally inherited adaptation also causes, indirectly, a genetically based change in a population. Gene-culture interactions of this kind mean that culture in animals is an evolutionary mechanism25 27.

The evolutionary power of this non-genetic mechanism is illustrated by strong evidence suggesting that behaviourally based gene-culture interactions of this kind may have generated the divergence of killer whales into several different types. Historically considered to be variants of the single species Orcinus orca, these “ecotypes” are so distinct that they may be approaching division into separate new species25.

Image credit: Damien Sanders ©

Summing up

Collectively, the examples of animal biology we have described establish something quite remarkable about animal adaptation: the responses of organisms faced with demanding or threatening environmental conditions can be influenced by the nature of those conditions, such that they can generate adaptations that are appropriate to the threat. This is in contrast to what for decades has been assumed to be the sole mechanism; variations in phenotype being generated by random genetic mutation. It now seems, therefore, that there are both random and non-random ways to produce the phenotypic variations that natural selection can act upon, causing adaptation and evolution. As understanding of how genes work emerged from the 1950s onwards it became difficult to conceive a mechanism by which genetics could accept information from the environment; the action of genes appeared well and truly one-directional. Political concerns may also have affected serious consideration of direct environmental influence on phenotype because the idea can be misinterpreted and wrongly applied, for example with regard to intelligence. “Nature not nurture” became a dogma in evolutionary biology.

Image credit: Hans Etholen https://pixabay.com/users/hve56-19607712/

In the early 21st century a measurable shift in thinking occurred. Research publications concerning extension of the evolutionary synthesis increased steeply after publication of Dr Mary Jane West-Eberhard’s book, “Developmental Plasticity and Evolution”28 in 2003, and as, concurrently, new techniques in molecular genetics research became available, enabling new understanding of epigenetic phenomena. The examples described here were selected to illustrate what has been added to evolutionary knowledge, and the consequent relaxation of restraints historically demanded by the MES.

It is not that the MES is being rejected; its mechanism remains largely correct and its evolutionary influence very important. However, the known mechanisms and consequent possibilities of evolution are expanding substantially, not least by advances in understanding of the molecular mechanisms of adaptation. Epigenetics is one example of this, another is processes of phenotypic alteration caused by changes in the combinations in which multiple genes are expressed rather than by mutational changes to the genes themselves29.

”It is not that the MES is being rejected, however … ”

Adaptation and evolution being responsive to the environment presents new possibilities to ecology and evolutionary biology, it may mean that living things have more capability to counter environmental threat than was previously believed. At a time when life on Earth faces extreme threat from environmental change, that may be a source of hope.

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