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Microbes on the Mind

Singers, songs and the more-than-individual holobiont

When you take an evolutionary view of Earth, an astonishing reversal takes place. Suddenly, things that you think of as real—this cat over here, my cat, whose fur I can stroke—become the abstraction, an approximation of flowing, metamorphic processes, processes that are in some sense far more real than the entity I am stroking.

When you take an evolutionary view of Earth, an astonishing reversal takes place. Suddenly, things that you think of as real—this cat over here, my cat, whose fur I can stroke—become the abstraction, an approximation of flowing, metamorphic processes, processes that are in some sense far more real than the entity I am stroking.

– Timothy Morton

I recently joined a virtual meeting on holobionts, microbiota and concepts of individuality in biology, organised by Thomas Pradeau of the University of Bordeaux . This meeting was part I of a series bringing together biologists and philosophers to debate the conceptual challenges currently faced within biology regarding individuality. Knowledge of the essential role that resident microbes play in maintaining the functional integrity of animals has generated a thorny challenge: the individual seems to be a composite. It is shaped and maintained by multiple genomes in continuous metabolic exchange. Where boundaries were once clear—a cell or skin membrane, a species, a genome—they are now queered. Biologically speaking, it has become unclear what—or who—an individual is, and where—and when— its boundaries can be drawn.

One area of biology where the notion of individuality has been central is evolutionary biology. In the Modern Synthesis, an individual is a unit of selection, a genomically coherent whole who is born into an environment and is better or less well adapted to that environment—it is more or less fit. Fitter individuals leave more offspring, thus replicating and recombining their winning genomic package. Evolutionarily speaking, an individual is a unit on which natural selection acts.

The holobiont—the composite organism comprised of microbial communities plus their animal or plant host—has been difficult to integrate into evolutionary theory. Mechanistic explanations of evolution by natural selection rely on approaching the biological world as one of individuals with strict boundaries and replicable genomes. Holobionts—who, genetic speaking, include the hosts’ genes plus the genes of all its microbial community—are  a problem here. It is not easy to draw clear genetic boundaries around the entity that is host-plus-microbiota, particularly given that the microbiome—the genetic composition of the microbiota—varies over the lifespan of the host.

At the meeting, one particularly lively discussion thread revolved around Ford Doolittle’s theory “It’s the song not the singer”, sometimes called ITSNTS, which proposes an evolutionary viewpoint beyond selection acting on individuals (1). Doolittle suggests conceptualising as units of natural selection the functional metabolic bonds that make that holobiont possible—not the organism as a thing. That is to say, selection would be construed to operate at the level of patterns of co-metabolism between the host and its microbiota. It is evolution beyond reproduction. Patterns get perpetuated because they create a niche, an environmental opportunity for organisms to grow into; and the most ‘attractive’ patterns persist—patterns most ‘successful’ at being re-used, we could say (if we inhabit words in elasticated ways). In ITSNS, evolution is seen to operate through differential persistence of patterns (songs), not through differential reproduction of organisms (singers). This, argues Doolittle, actually fits better the expression ‘survival of the fittest’- which never was ‘reproduction of the fittest (2).

The theory is contentious, and the discussion—past 10pm at night European time—got lively. Ecologist Joan Roughgarden expressed a pragmatic point of view—that this theory, which she sees as one of a series of projects aimed at replacing things (taxa, singers) with processes (patterns, songs), is bound to fail because people care about things, not functions. They care about animals: not about the metabolic patterns that sustain them. Which brought me to think of a quote I came across a few years ago, in Timothy Morton’s ‘The Mesh’(3):

“(…) The trouble is that when you take an evolutionary view of Earth, an astonishing reversal takes place. Suddenly, things that you think of as real—this cat over here, my cat, whose fur I can stroke—become the abstraction, an approximation of flowing, metamorphic processes, processes that are in some sense far more real than the entity I am stroking. (…) The real thing is the evolutionary process—the cat is just an abstraction! The discovery of evolution is nothing less than a Copernican revolution, in which what we take to be immediate and real turns out to be an abstraction of a deeper reality”.

Returning to the holobiont meeting, where we were discussing ways of theorising evolution rather than reversals in perceptual pathways—Scott Gilbert argued that song and singer are crucial. While co-metabolic patterns between host and its community of microbes (songs) are the glue of holobionts, sometimes a singer—a particular species—is critical to the existence of a holobiont. That is to say, some host-microbial partnerships are highly specific at a species level. For example, take the symbiotic partnership between the Hawaiian bobtail squid, Euprymna scolopes, and the bacterial consortium Vibrio fischeri. The bobtail squid is a nocturnal marine creature; as it travels under the light of the moon or stars, it naturally casts a shadow onto the seafloor, which—rather inconveniently—can be detected by potential predators or prey. But the bobtail squid has evolved a means of disrupting the light of its own shadow. In symbiotic partnership with luminescent bacteria which colonise its ventral surface and cast their own light onto the seafloor, the holobiont squid can travel the sea undetected. The bobtail squid ‘recruits’ these bacteria from the surrounding seawater—they are not encoded in its genome. Many other bacteria live in the water and enter the squid, but only vibrio is allowed to stay—other incomers are killed or expelled. Thus sometimes a song is one singer. Or rather, an exclusive and wondruous duet.

I have never seen a bobtail squid in the flesh, but having heard about it a great deal, it inhabits my imagination. This creature who is not born but acquired, who has evolved to be a composite of lit bodies, so contingently and imperfectly made. The baroque nature of this multi-species arrangement fills me with wonder;  the bobtail squid has become exquisitely adapted to its way of life by selectively gathering place and others into itself, time and time again. Animals are unique, unfinished tales of body-in-development meeting place and making itself anew— following well-trod pathways, yet differently every time. One moment I gaze at the living, purring cat in front of me as an independent entity with unique will, an ephemeral wonder of flesh and bone and sentience other than mine.

Another moment it yawns, and a glimpse of sharp canines leaps my thought to its wild kin, tearing daily into flesh and bone—and the long, webbed thread of Life that binds me and this cat as one. It can feel like a mind game to pin down this cat as abstraction, in order to reveal as real the evolutionary flow of Life of which cat is but a stable moment.  But embracing the two viewpoints has experiential power for me. In my day-to-day life as a citizen, when I pay careful enough attention to a singer, and another, and another,  I start to glimpse details of the song. And that… it has nothing and everything to do with theories of individuality. 

LINK TO FULL VIDEO OF ERC-IDEM MEETINGS

BIBLIOGRAPHY:

1. Doolittle WF, Booth A. It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos. 2017 Jan;32(1):5–24.

2. Doolittle WF, Inkpen SA. Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking. Proc Natl Acad Sci. 2018 Apr 17;115(16):4006–14.

3. Morton, Timothy. The Mesh. In: LeMenager S, Shewry T, Hiltner K, editors. Environmental criticism for the twenty-first century. New York: Routledge; 2011. p. 1–16. (Routledge interdisciplinary perspectives on literature).