New trends in evolutionary biology: biological, philosophical and social science perspectives

Many of the most important evolutionary variations that generated phenotypic adaptations and originated novel taxa resulted from complex cellular activities affecting genome content and expression. These activities included: (i) the symbiogenetic cell merger that produced the mitochondrion-bearing ancestor of all extant eukaryotes; (ii) symbiogenetic cell mergers that produced chloroplast-bearing ancestors of photosynthetic eukaryotes; and (iii) interspecific hybridisations and genome doublings that have generated adaptive radiations and new species of higher plants and animals. Adaptive variations have also arisen by horizontal DNA transfers (frequently involving infectious agents), by natural genetic engineering of coding sequence DNA in protein evolution (e.g. exon shuffling), and by mobile DNA rewiring of transcriptional regulatory networks, such as those essential to viviparous reproduction in mammals. In the most highly evolved multicellular organisms, we now know that biological complexity scales with ‘non-coding’ DNA content rather than with protein-coding capacity in the genome. Coincidentally, we have come to recognise that ‘non-coding’ RNAs rich in repetitive mobile DNA sequences function as key regulators of complex adaptive phenotypes, such as stem cell pluripotency. The intersections of cell activities and Read-Write genome modifications provide a rich molecular and biological foundation for understanding how ecological disruptions can stimulate productive, often abrupt, evolutionary transformations.

I outline an approach to measuring biological information where ‘information’ is understood in the sense found in Francis Crick’s foundational contributions to molecular biology. Genes contain information in this sense, but so do epigenetic factors, as many biologists have recognised. The term ‘epigenetic’ is ambiguous, and I introduce a distinction between epigenetic and exogenetic inheritance to clarify one aspect of this ambiguity. These three heredity systems play complementary roles in development and evolution.

The construction of the ‘Modern Evolutionary Synthesis’ in the mid-twentieth century involved the exclusion of soft inheritance – the inheritance of the effects of developmental modifications – and, by implication, the possibility of any form of ‘Lamarckian’ evolution. However, in later decades, discoveries of molecular mechanisms that can support such inheritance led to a broadening of the notion of biological heredity. After discussing the historical context in which this change occurred, I present an extended notion of inheritance, focusing on epigenetic inheritance and its underlying mechanisms. I examine the evidence for the ubiquity of epigenetic inheritance, present models of population epigenetics, and discuss the involvement of epigenetic inheritance in adaptive evolutionary change and macro-evolution. I argue that considering the many evolutionary consequences of epigenetic inheritance requires an extension of the evolutionary synthesis beyond the current neo-Darwinian model.

Multicellular organisms do not live in an axenic world, but in one populated by microbes. Indeed, it can be argued that what we see as an individual animal or plant is in fact biologically a composite of the animal/plant and associated microbes. The individual generated is not simply a passive result of associations, but commonly an integrated one. Animal/plant development occurs in concert with microbes, and microbiome constitution is determined in part by the animal/plant, which may select particular microbes. In my talk I will focus on the most integrated symbioses, where microbes pass from a mother to offspring and thus represent part of host heredity. I will discuss why hereditary symbiosis evolves, how it widens our view of evolutionary processes, and how it affects what we mean by an ‘individual’.

Medicine and physiology are multi-level disciplines. So is physics. From physics we learn that ordered properties at high levels co-exist with randomness at lower levels. Molecules in organisms must obey the same principles. Stochasticity at low levels does not therefore exclude order at higher levels. Organisms enlist stochasticity in their development of functional behaviour, through restraints exerted by higher over lower levels. The physics of organisms must therefore interact with their genomes to produce the phenotype^1,2. Reverse engineering from physiological models is then required to understand genotype-phenotype relations³. There is no privileged level of causality⁴, nor privileged level of selection⁵. Evolution involves interaction between several processes at multiple levels, as Charles Darwin also believed^5,6. Without understanding these interactions, gene-centred approaches will continue to produce disappointing results in healthcare^7,8, including trans-generational disease risks.  

1. Alvarez-Buylla ER et al. 2016. Bioscience 66, 371-383.
2. Edelman DB et al. 2016. Progress in Biophysics and Molecular Biology (doi:10.1016/j.pbiomolbio.2016.06.007) 
3. Noble D. 2011. Interface Focus 1, 7-15.
4. Noble D. 2012. Interface Focus 2, 55-64. 
5. Noble D. 2016 Dance to the Tune of Life. Biological Relativity. CUP.
6. Noble D. 2015. Journal of Experimental Biology 218, 7-13. 
7. Editorial, 2010 Nature 464, 649-650.
8. Joyner MJ, Prendergast FG. 2014. Journal of Physiology 592, 2381-2388.

A longstanding tension exists in evolutionary biology between behavioural ecology – in which organisms are treated as having adaptive, fitness-maximising agendas; and population genetics – in which such notions are decried as naïve ‘anthropomorphism’ and are widely rejected. I explore the formal and scientific justification for evolutionary anthropomorphism and consider its application to the understanding of adaptive design at the level of genes, individuals and societies.

The capacity of organisms to respond in their own lifetimes to new challenges in their environments probably appeared early in biological evolution. At present few studies have shown how such adaptability could influence the inherited characteristics of an organism’s descendants. Nevertheless such effects on biological evolution are likely to have been important and when they occurred accelerated the pace of evolution. Ways in which this might have happened have been suggested many times since the 1870s. I shall review these proposals and discuss their relevance to modern thought.

It is striking that evolutionary biology often uses the language of intentional psychology to describe the behaviour of evolved organisms, their genes, and the process of natural selection that led to their evolution. Thus a cuckoo chick ‘deceives’ its host; a worker ant ‘prefers’ to tend the queen's eggs to those of other workers; a swallow ‘realises’ that winter is approaching and ‘wants’ to escape it; an imprinted gene ‘knows’ whether it was inherited paternally or maternally; and natural selection ‘chooses’ some phenotypes over others. 

This intentional idiom is a symptom of a broader way of thinking about and modelling evolution, which I call ‘agential’. This involves treating evolved entities, paradigmatically individual organisms, as if they were agents trying to achieve a goal, namely maximisation of reproductive fitness (or some proxy). The use of rational choice models, originally intended to apply to deliberate human action, in an evolutionary context, is one symptom of agential thinking. 

I offer a cautious defence of agential thinking in evolutionary biology. I argue that this mode of thinking does genuine intellectual work, and is not ‘idle metaphor’. The key point is that attributions of agency presuppose a ‘unity of purpose’. Therefore an evolved organism can only be treated as agent-like to the extent that its phenotypic traits have complementary rather than antagonistic functions, i.e. contribute to a single overall goal. Where this is not the case, e.g. because of unresolved intra-genomic conflict, the metaphor of agency ceases to be applicable.

In the last decade niche construction has been heralded as the neglected process in evolution. But niche construction is just one way in which the organism’s interaction with, and construction of the environment, can have potential evolutionary significance. This constructed environment not just selects for, it also produces new variation. Nearly three decades ago, and in parallel with Odling-Smee’s book chapter ‘Niche-constructing phenotypes’, West and King introduced the ‘Ontogenetic Niche’ to give the phenomena of exogenetic inheritance a formal name. Since then a range of fields in the life sciences and medicine has amassed evidence that parents influence their offspring by means other than DNA (parental effects). Diverse scientists use different theoretical constructs for overlapping sets of processes, all of which show one way or another how heritable variation can be environmentally induced and developmentally regulated. Here I propose the concept of ‘developmental niche construction’ as a framework to integrate findings from fields ranging from molecular biology to developmental psychology. It elucidates how a diverse range of mechanisms contributes to the transgenerational transfer of developmental resources. This talk will explore the overall significance of these developments in the life sciences, and particularly how they advance the ongoing integration of development, heredity, ecology, and evolution.

In recent years, far from arguing that evolutionary approaches to our own species permit us to describe the fundamental character of human nature, a prominent group of cultural evolutionary theorists has instead argued that the very idea of 'human nature' is one we should reject. It makes no sense, they argue, to speak of human nature in opposition to human culture. But the very same sceptical arguments have also led some thinkers – usually from social anthropology – to dismiss the related idea that we can talk of human culture in opposition to human nature. 

How, then, are we supposed to understand the cultural evolutionary project itself, which seems to rely on a closely allied distinction between 'organic' and 'cultural' evolution? This talk defends the cultural evolutionary project against the charge that, in refusing to endorse the concept of human nature, it has inadvertently sabotaged itself.

Scholars from a diverse range of disciplines disagree on what human nature is, what it could be, or even if there is one. There is no single ‘best’ discourse on, or mode of approach to, human nature. However, in the context of what we know about the evolutionary history, anthropology, and biology of Homo sapiens sapiens it is clear that an evolutionary approach should be among the principal modes of inquiry. At present we are faced with a few different narratives as to exactly what such an evolutionary approach entails. However, one point is clear: we need a robust and dynamic theoretical toolkit in order to develop a richer, and more nuanced, understanding of the cognitively sophisticated genus Homo and the diverse sorts of niches humans constructed and occupied across the Pleistocene, Holocene, and into the Anthropocene. In this talk I review current evolutionary approaches to ‘human nature’ and argue that we benefit from re-framing our investigations via the concept of the human niche and in the context of the Extended Evolutionary Synthesis (EES). In providing an overview of human evolution and the human niche I illustrate the benefits of moving the discourse on human nature(s) to an integrated evolutionary approach incorporating processes of the Extended Evolutionary Synthesis. This is not a replacement of earlier evolutionary approaches but rather an expansion and enhancement, a broadening of our toolkit and the landscape of inquiry. I offer brief examples from human evolutionary histories in support of these assertions.

By the mid-twentieth century the behavioural sciences could offer only the sketchy beginnings of a scientific literature documenting evidence for cultural inheritance in animals – the transmission of traditional behaviours via imitation and other processes of learning from others (social learning). By contrast, recent decades have seen a massive growth in the documentation of such cultural phenomena, driven by long-term field studies and complementary laboratory experiments. Here I first offer an overview of the major discoveries in this field, which increasingly suggest that this ‘second inheritance system’, built on the shoulders of the primary genetic inheritance system, occurs widely amongst vertebrates and possibly in insects and other invertebrates too. Its novel characteristics suggest it should have major implications for our understanding of evolutionary biology. Two major questions arising are accordingly addressed. One concerns the extent to which this second system echoes or differs from the principal properties of the primary evolutionary system described in the neo-Darwinian synthesis of the twentieth century and its extensions under discussion at this meeting. A subsidiary issue here is how the answers may differ much according to whether the focus is on the massively cumulative cultural evolution distinctive of our own species, or on the forms of cultural transmission documented for other species. The second major, and related, question concerns the extent to which the new discoveries about animal cultural transmission extend evolutionary theory, either in addition to or through interaction with the primary, genetically based inheritance systems.

Recent humans are biocultural organisms. Our worldwide distribution and status as the lone surviving species of our genus signal a level of evolutionary success often explained by both biological and cultural mechanisms. A bio-behavioural package of traits that co-exist in Homo sapiens, including large brains and bodies, small teeth and jaws, extensive cooperative care, a great deal of developmental plasticity, and an extensive amount of niche construction, are variously implicated in our success or seen as its result.

It is broadly accepted that recent humans are ‘different’, particularly in the extent of our cultural interventions, than our earlier hominin forebears. But whether this is a difference in kind or degree, how far back that difference stretches, and whether those outcomes modifiable over an individual’s lifetime are important to human evolution is open to debate. Regardless of whether we accept exogenetic changes – including developmental niche construction – as consistent with an extension of, or break with the evolutionary synthesis, Homo erectus has often been proposed as the locus at which more ‘human like’ modes of behaviour (and presumably more biocultural evolution) is seated.  But the paucity of the fossil record and the tenuously established links between bones and behaviours of interest limit our ability to test these assertions. I review the evolution of Homo and recent attempts to locate the transition to a biocultural organism with new data and by both working back from recent humans through archaeological time and working forward from ancestral genera. 

In his book The Variation of Animals and Plants under Domestication Darwin used domestication as a model system to explore his theories about the role of natural selection in evolution. Gregor Mendel used peas to trace the rules of heredity that formed the basis of the science of genetics, and that, when combined with Darwinian evolution, formed the basis of the Modern Synthesis. It seems only appropriate for domestication to serve once again as a model system for assessing how recent insights into the role of multiple shaping processes and forms of inheritance can be incorporated into an extended understanding of evolution. This presentation explores the value of domestication in evaluating core assumptions that differentiate the classical Modern Synthesis and the Extended Evolutionary Synthesis including: 1. reciprocal causation, 2. developmental processes as drivers of evolutionary change, 3. inclusive inheritance, and 4. the tempo and rate of evolutionary change.