From one to many: Parallels between multicellularity and social behaviour – Fellows’ seminar by Vidyanand Nanjundiah

7 October 2019

“Highly organised group life is common to humans and cells, but we view the phenomenon very differently in the two cases. There are two types of explanations for the evolution of group life. The first is a gene-based explanation and is standard in biology. It invokes natural selection acting on the consequences of new genes that made sociality possible. The second explanation stresses the novel (‘emergent’) behaviours that simple interacting units can exhibit when put together. It is common in the physical sciences and – curiously – in the social sciences” said STIAS fellow Vidyanand Nanjundiah, of the Centre for Human Genetics in Bangalore.

STIAS fellow Vidyanand Nanjundiah during his seminar on 3 October 2019

“Primitive soil amoebae known as cellular slime moulds are a well-studied example. They open up the possibility of inferring what steps might have underpinned the transitions in the past,” he continued. “These amoebae display the transition from individual to group living as part of their normal life cycle. One can view them as multicellular organisms and social beings at the same time.”

“I’m interested in understanding what the relative merits of gene-based and individual-based explanations are for the origin of their unusual lifestyle? And what lessons we can draw from that for understanding group life in general?”

Nanjundiah started by outlining the unique level of explanation that biology requires, mainly due to the theory that evolution works by natural selection, which we owe to Darwin and Wallace. He also outlined the major stages in the development of evolutionary theory from Darwin onwards.

“After an initial buzz, the notion of natural selection became unpopular amongst scientists,” he said, “only for interest in it to pick up once again from the 1930s onwards.”

Counting children to counting genes

“Natural-selection can be roughly described as being based on ‘counting children’. The reproductive success of an individual can be measured in terms of the number of children he or she has. If people differ in reproductive success on account of some trait that can be passed on to children, counting the number of children is a way of working out which traits are more likely to spread over many generations.”

“That way of looking at natural selection was gradually supplanted by the opinion that ‘counting genes’ was a better way of understanding how natural selection worked than ‘counting children’. The notion of the so-called ‘selfish gene’ is all about ‘counting genes’,” he added.

“There were many reasons behind the changed viewpoint. Firstly, in sexually reproducing creatures – like many plants and animals including ourselves – children are not faithful replicas of their parents. In other words, parents do not pass on copies of themselves. However, parents do pass on copies of their genes. In terms of traits, we inherit the capacity to exhibit our parents’ traits, and those capacities depend on the activities of genes. Secondly, there are situations in which genes seem to take on a life of their own. That is, genes can spread even at the cost of hindering the reproductive success of their bearers. Obviously, in such situations ‘counting genes’ is a better way of following the process of evolution than ‘counting children’. Thirdly, there was the curious example of ants, bees and wasps, which seemed to behave altruistically – they seemed to favour helping someone else to have children over having their own child. Obviously, ‘counting children’ cannot account for the evolution of that sort of behaviour. The explanation seemed to lie in an unusual form of reproduction followed by these insects. Because of it, under certain circumstances, females, who are workers, have a better chance of passing on their genes by acquiring sisters than by having sons or daughters. And indeed they spend all their time helping their mother to lay eggs, some of which are females. That gives them a substantial ‘gene count’ in the next generation, even though their ‘children count’ is zero.”

“In short, female worker bees don’t have children but help the queen to have them. It’s an economic enterprise to keep up the hive by producing sister bees which are genetically closer to each other (75%) than the mothers and daughters (50%). It appears that the same explanation might hold good in the case of ants and wasps.”

“Worker bees also indulge in suicidal behaviour for the good of the hive,” continued Nanjundiah. “They sting an intruder that threatens the hive and, in the process, die themselves”.

He added that there are also policing activities – preventing other workers from reproducing successfully – that also point to the gene-centred view as being correct. Even before people had thought of the example of the social insects, some scientists said that ‘counting genes’ was the sensible way of understanding natural selection.”

“By 1950, the gene-centred view of natural selection, and, in fact, of evolution generally, became firmly established in the minds of most biologists. It came to be called the neo-Darwinian theory of evolution, or sometimes the Modern Synthesis. It rested on the links that had been established between heredity, genes, proteins, and traits,” continued Nanjundiah.

But not the whole story

But although genes and genetic identity are undoubtedly important, they are not the only factors at work. “Genes certainly impact on the wellbeing of the organism. It has become clearer, however, that despite the fact that the capacity to express innate tendencies is transmitted via genes, many other factors bear on the traits expressed by organisms.”

“When a unit makes way for a second unit that is made up of many members of the first, the notion of individuality, which initially referred to the ‘one’, now refers to the ‘many’. The transition is central to language, art and music, and also to physics and chemistry. A major evolutionary transition that belongs to the same category was the origin of multicellular life about 650 million years among the eukaryotes (creatures like ourselves, with cells containing nuclei, unlike bacteria). Amazingly, there are some groups in which the one cell-to-many cells transition keeps happening to this day in every life cycle. This opens up the possibility that by studying features of the transition as it is taking place before our eyes, we may be able to guess what factors were responsible for its happening all those millions of years ago. In particular, it enables us to compare the relative merit of ‘counting children’ and ‘counting genes’ as explanations. Such studies raise the interesting hypothesis that pre-existing cellular properties, rather than newly arisen genetic capabilities, may have played a significant role in the transition. My project is aimed at examining this hypothesis critically.”

Nanjundiah used the case of the cellular slime moulds as an illustration. In these organisms, starved amoebae come together to form an aggregate. Aggregation seems to be a defensive response to starvation, but matters are not straightforward. Within the aggregate, the amoebae display a division of labour that is as drastic as that seen in the social insects. Amoebae that were previously undifferentiated, now turn into dead stalk cells or live spore cells, and the stalk holds up the spores and helps them to spread far – with luck, to a place where food is available. This means that like worker insects, stalk cells do not themselves reproduce, but, in an apparent example of altruism, aid the reproduction of spores (which are analogous to the queen). Clearly, the amoebae that become stalks have no ‘children’ whereas those that form spores, do. This makes it appear that ‘counting children’ is the correct formula to use. But there is a problem. The amoebae that join to form an aggregate can have very different genes: there is no guarantee that an amoeba that forms a spore, preferentially aids amoebae that carry a substantial proportion of its own genes. Rather, it appears that multicellular living could involve complex interactions between cells that result in some dying and others surviving, without genetic relatedness playing a major role. But if that is the case, don’t the genes of the amoebae that die, disappear? No, because who dies and who lives can vary from case to case. In one group, amoebae with gene-set A may have a higher chance of surviving than amoebae with gene set B; in another group, B may do better than A.

Interestingly, subsequent work on insects shows that there too, ‘counting genes’ may not be the full story.

In discussion, Nanjundiah pointed to the challenges of language within the social biology field – pointing out that words like ‘suicide’ and ‘altruism’ have very loaded, emotional connotations. “Language is a big issue in sociobiology,” he said. “Different people use different definitions. We tie ourselves in knots with words.”

“Multicellular organisms and social behaviour definitely have features in common,” he concluded. “Genes are important, nothing is possible without genes, but it’s simplistic to think only in terms of a gene or genes for social behaviour. Single-cell organisms gave way to multicellular organisms but some still survive – so many stable outcomes are possible.”

Michelle Galloway: Part-time media officer at STIAS
Photograph: Christoff Pauw

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