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Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral and Symbolic Variation in the History of Life. Jablonka and Lamb 2014

I’ve been reading some interesting books lately! This one was a hard one to put down as the authors provided a number of really engaging case-studies to support an “extended evolutionary synthesis”. I thought I would give a brief synopsis and discuss some of the arguments Jablonka and Lamb made in their excellent book entitled: “Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral and Symbolic Variation in the History of Life”

In their updated book, Jablonka and Lamb argue that the Modern evolutionary synthesis, developed in the 1960s, is lacking and is not sufficient in explaining evolutionary change on its own. In particular, they suggest that our understanding of heredity and the generation of phenotypic variants that is based mainly on genes is incomplete and can be misleading. They argue that we need to be thinking about alternative modes of inheritance, different ways phenotypic variants are created and the interactions between different inheritance systems and the environment to fully understand evolutionary change. They suggest that there exist four inheritance systems: genetic, epigenetic, behavioural and symbolic/cultural, although they recognise that they are not necessarily mutually exclusive. In the chapter on the genetic inheritance system, which is the major foundation of the modern evolutionary synthesis, they argue that genes alone are not sufficient to explain all evolutionary change because genes often do not map neatly to phenotypes and mutations are too slow for rapid evolutionary changes to proceed. Particularly problematic are the ideas that mutations are often random and deleterious and given these points it is difficult to explain how organisms can adapt quickly to their environment. Alternative inheritance systems and phenotypic plasticity are therefore extremely important in evolution. In this chapter they challenge a few of these ideas about mutations. For example, it may not generally be the case that mutations are random and they provide evidence that, in light of environmental stresses, mutations can occur non-randomly in the genome and that certain genes appear to be bigger targets than others. Although they do not deny that selection on genetic variants is extremely important in evolution and they do indeed discuss the role of environmental stressors in exposing hidden genetic variation, which is a very important point,  they do make it fairly clear that our current view and disproportionate emphasis on genes is not justified for reasons outlined below.

Discussion of the epigenetic inheritance system was a major component of the book and was threaded through different inheritance systems (particularly behaviour). Epigenetic inheritance is when phenotypic variants, not stemming from changes to DNA sequences, are transmitted to subsequent generations. This could be through changes in germ line cell methlyation or siRNA transfer, but also through the perpetuation of environments across generations that lead to similar developmental changes in the next generation. This could be important in light of developmental canalisation and genetic assimilation if selection is strong and consistent.   Jablonka and Lamb discuss a huge number of interesting mechanisms that lead to epigenetic changes including DNA methlyation (silencing of gene expression), chromatin remodelling, prions (proteins that change the conformation of other proteins to “look” more like them) and more interestingly small RNA’s (e.g siRNA and miRNA).  In their new chapter they discuss some amazing examples of the role epigenetic effects can play in evolution. Two that I was particularly fascinated by were the role of maternal care in rat pups and odour imprinting in C. elegans because these were also directly relevant to the behavioural inheritance system. In the first example, Jablonka and Lamb reference a study on rats which showed how maternal care (licking and grooming) of offspring influences their behaviour as they age. Offspring become more resistant to stress and are more exploratory. Interestingly, offspring raised by these caring mothers are also more likely to lick and groom their offspring and thus the behaviour is perpetuated. These behaviours seemed to be linked with differences in DNA methylation and DNA associated proteins which likely change gene expression. In the second example, C. elegans that were raised on a particular odour during a larval stage where more likely be attracted to this odour as adults and increased their egg production in response to it. This behaviour does appear to be transferred to their offspring, but if exposure to the odour does not persist it lasts for only a few generations. However, surprisingly, if the odour exposure is consistent (i.e. exposure occurs across 4 generations) then it can be sustained and inherited for up to 40 generations! Although the epigenetic mechanism involved here are not known, given that they lack DNA metlyation, they suggest it may be linked to sRNA.

One particularly relevant and interesting part of the book was on the role of learning and innovation in evolutionary change.  They discuss a few interesting examples of how social learning may facilitate phenotypic evolution. Innovative behaviour or trial and error learning may lead to an individual learning to solve a new problem, social learning can then lead to transgenerational inheritance of this “acquired trait”. They provide some well known examples here including how Israeli black rats learn from adults about how to eat pine cones and thus the behaviour can be transmitted across generations and the rapid and extensive spread of bottle top removing by tits in the UK.  These behavioural innovations are acquired traits that are passed between generations and interestingly transmission can not only occur vertically (i.e. parents to offspring) but also horizontally (between totally unrelated individuals).

In the chapters on symbolic or cultural inheritance they discuss a lot about how cultural traditions can be transmitted and how small additions/changes can leading to new variants that are slowly accumulated and incorporated into existing traditions. They also talk quite a lot about the evolution of language.  Probably one of the most interesting things about the book was that these different inheritance systems are incredibly interconnected and Jablonka and Lamb really highlighted the constant feedback loop between selection and the environment. They argue that often “genes are follows” so changes in environmental niches change the environment and the selection pressures individuals experience and selection can subsequently lead to genetic evolution to fine tune adaptation to the new environment. They highlight a few cool examples, but the most interesting one was the apparent spread of alleles that allowed humans to digest lactaose that were followed by changes in agricultural practices.

Throughout the book they discuss how each of these inheritance systems can lead to evolutionary change while “holding” all the other inheritance systems constant and how each of the different inheritance systems influence each other. They provided metaphorical examples about how each system can lead to phenotypic evolution. For example, when there is no genetic variation in the system how can phenotypic evolution occur? While obviously unrealistic, these examples do highlight how the fundamentals of evolution (variation, heredity and selection) can lead to changes in the frequency of phenotypes over time. They also discuss several criticism of the importance of the three additional inheritance systems in evolution, and a point that was brought up often was about the stability of these phenotypic changes in the epigenetic, behavioural and cultural realms. While I think this is certainly a valid point, and it is clear that some cases of epigenetic effects are not necessarily long term, there is indeed evidence that these effects can be extremely long-term and theoretical works has shown that they can influence evolutionary dynamics (e.g. rate sod genetic evolution). In addition, I do think that a similar argument could be made about genetic variants. If we think of evolution as simply changes in allele frequencies over time then there is nothing wrong about allelic variants fluctuating back and forth over time (e.g. frequency-dependent selection at a locus). Would we not call this evolution? I think an important distinction that needs to be made is the difference between genetic evolution and phenotypic evolution. Of course, if you view evolution as changes in allele frequencies over time then you probably won’t accept that epigenetic, behavioural and cultural inheritance systems are all that important except in changing the environment in which selection acts. However, if you distinguish between genetic and phenotypic evolution, which Jablonka and Lamb show sort of hint at, both can occur independent of one another and I think this helps to clarify things.

Overall, I found this book to be extremely interesting, filled with new ideas, new ways of thinking about evolutionary change and stuffed with fascinating examples. Their new updated chapter was refreshing and involved a foray into the new developments in the field. Given the evidence presented in the book, even though we are still just at the tip of the iceberg, they do indeed provide a compelling argument for an “Extended Evolutionary Synthesis” in evolutionary biology.

Lizards learn from their elders too!

Social learning—the ability of an animal or human to acquire information by learning from the actions of others is a short-cut to solving many of life’s problems or simply acquiring information more quickly. Just think back to when you got your first video recorder all those years ago, or satellite TV, with a remote with more functions than a space shuttle. Who wants to spend hours poring over an instructional manual when an older person can show you what you need to know in a matter of a few minutes? That way you can get to watching and recording your favourite programs in no time.

Social learning was always thought to be the hallmark of highly intelligent primates and birds. And indeed, we see chimps and crows learning to use tools by watching group members in action. More recently, social learning has been documented in a much wider range of species including insects, turtles, fishes and tadpoles. This should not be all together surprising, because natural selection should select for animals capable of rapidly acquiring essential information that will ultimately give them the edge over rivals.

Martin and I teamed up with Richard Byrne from the University of St. Andrews in Scotland, to conduct the first test of social learning in a lizard which has recently been published the the Royal Society journal Biology Letters. We used our favourite lizard, the Eastern Water Skink (Eulamprus quoyii), since we have been working with them since 2010 and we have previously shown that they can learn quite rapidly. We used two groups of lizards based on their age: ‘old’ lizards that were about 5 years old and ‘young’ lizards that were 1.5-2 years. We began by training a group of demonstrators to solve a task that involved them having to flip a lid off a dish in order to acquire a nice juicy mealworm. We then randomly allocated lizards either to a social learning treatment where they would see a demonstrator conduct the task, or to a control, where they would see another lizard but without them doing the task. The lizards were separated from each other by a piece of see through plastic. Both young and old lizards were put through two different tasks differing in their complexity. Check out the video at the bottom of the post to see a lizard in action!

A lizard with the two food dishes

A water skink with the two food dishes it had to choose from.

Our favourite water skink...enjoying the beach!

Our favourite water skink…enjoying the beach!














The results were somewhat surprising. Old lizards did not appear to use social information in any significant way and learnt to solve the tasks at much the same speed as the control group. Young lizards on the other hand, did pay attention to social information and learnt to solve the second task faster than both the control group, and old lizards. There may be several reasons for this interesting result. Young lizards may stand to benefit more than older lizards by paying attention to the life lessons of other lizards. Alternatively, they may also have more opportunity for social learning because adults are less tolerant of rivals and more likely to chase adults away than they would a juvenile. Lizards can now be added to the growing list of animals capable of social learning. Furthermore, they can also be added to the much smaller list of animals in which we know that social learning is age-dependent.

If you’re interested in reading more about our paper you can access it from my publications page HERE or visit the link below:

Age-dependent social learning in a lizard, Biology Letters 2014, Daniel W. A. Noble, Richard W. Byrne and Martin J. Whiting,



Athletic lizards: Sex, hormones, and physical performance

When it comes to animal athletics lizards have been model systems for exploring the relationships between ecology and physical performance. Our two recent papers, one in the Biological Journal of the Linnean Society and the second in Behavioral Ecology add to the growing list of studies looking at functional performance in lizards.


Water skink basking on a log (Eulamprus quoyii)

Water skink basking on a log (Eulamprus quoyii)

In our first study, we explored the proximate underpinnings of physical performance in lizards and tested what might drive differences in performance between the sexes. Sex-dependent performance is found in many animals, including humans. Males tend to excel in activities such as running and jumping. The same is true for many lizards. But why are males better athletes than females? This is actually a very difficult question to answer because males differ from females in a number of different ways. For example, aside from hormone differences between the sexes, males are often larger than females and as a result differences in size can allow males to dominate in performance related activities.  One way to get around this is to control for size, but how can we do this? Well we could explore functional relationships in species that are not strongly sexual dimorphic because physiological traits that scale with size should be much more similar between the sexes. This provides a unique opportunity to explore how proximate mechanisms, such as hormones, affect the physical abilities of males and females and whether such physiological traits drive performance differences between the sexes.

Measuring lizard biting

Measuring lizard biting

Measuring lizard endurance on a human treadmill.

Measuring lizard endurance on a human treadmill.

Measuring lizard speed from a lizards eye view

Measuring lizard speed from a lizards eye view









In our recent paper published in the Biological Journal of the Linnean Society we tested whether a key hormone, thought to be different in males and females, was a driver of performance differences using our familiar and charismatic lizard species, the Eastern Water Skink (E. quoyii). The cool thing about E. quoyii is that males and females are of similar body size (at least in length). The notorious hormone I speak of above was testosterone. Testosterone is known to be an anabolic (build up) hormone, promoting muscle and body growth. It also affects a whole suite of other physiological parameters. We predicted that differences in circulating testosterone may be one reason why performance may vary between individuals and possibly explain any sex differences in performance. In our study we collected over 200 lizards and took measurements of their androgen levels (testosterone-like hormones) and tested whether: a) it varied between the sexes and b) whether it was positively related to performance in males and females. What we found was interesting. First, as expected males and females did not differ in body length, but did differ in mass and head size with males being heavier and having larger heads. We also found that males were far better performers than females. They ran faster, longer and bit much harder than females. However, surprisingly, we found no differences at all in the levels of circulating hormone concentrations between males and females and also found that it was not related to any of the performance traits. Despite this, we found huge variation in hormone levels, from individuals with virtually non-detectable levels to ones having orders of magnitude higher concentrations. We also found that androgen concentrations may not be related to performance in a simple linear way in males (although much more work needs to be done on this front). The jist of our results are that despite no differences in androgens males and females still differ substantially in their athletic abilities and that body size (at least length) and testosterone don’t seem to be the main reasons. However, we suggest that these differences may arise as a result of the development of different limb and head sizes, which contribute to running and biting performance that are likely organized differently among the sexes as they develop. This may have been a result of different sensitivities to androgens at key periods of growth of the limbs and muscle. The differences in the shape between the sexes suggest that differential selection on performance traits occurs between males and females. However, that is another story and for selection to result in evolutionary change these traits need to be heritable. But are they?

In our second study published in Behavioral Ecology, we explored whether running speed and endurance had additive genetic variance and showed evidence of being heritable (traits can be passed on from one generation to the next). Interestingly, we found weak evidence that sprint speed was heritable, but rather it appears to be strongly controlled by the phenotype of the mother. When a mother’s phenotype affects the phenotype of their offspring beyond their genetic contribution, this is called a maternal effect.  These can have very interesting effects on trait evolution. In contrast, running endurance showed reasonably high heritability suggesting that, if selection were to act on endurance, this trait has the potential to respond to selection.

You can read more about our work in the Biological Journal of Linnean Society and Behavioral Ecology by going to my publications page and clicking the relevant links.