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.