Re-thinking the theory of Evolution
How does evolution select the fittest “individuals” when they are ecosystems made up of hosts and their microbiomes? Biologists debate the need to revise theories.
Microbiome science has revealed the deep interdependencies of animals and plants on their microbial partners, prompting calls for an expansion of evolutionary theory.
Twilight falls on the Tanzanian plain. As the sky turns a deeper purple, a solitary spotted hyena awakens. She trots along the border of her clan’s territory, marking the boundary with a sour paste from under her tail. She sniffs a passing breeze for hints of itinerant males interested in mating, giving little attention to her stomach’s rumbling over the remnants of the previous night’s hunt or the itch on her flank. The lone hyena chooses what she will do next to make her living.
Except she is not alone. That paste she secretes is produced not by her own cells but by billions of bacteria housed within her scent glands. The scents on the breeze from potential mates also come from unique microbial concoctions. A diverse array of bacteria that line her gut are helping to break down her meal. Others assist her immune system in fending off the hordes of parasites and pathogens trying to invade her skin and other tissues.
Who precisely is it, then, trying to survive on the Tanzanian plain? Can we consider the fates of the hyena and the microbes within her independently? Or does their interaction form something new, greater than each part alone?
“We’ve underestimated the potential contribution of microbes to traits we’ve been studying for decades or centuries,” said Kevin Theis, a microbiologist at Wayne State University who studies the paste-making microbes of the hyena. “If the genes for these important traits are actually in the microbiome and not the animal itself, then we need to take a systems-level approach and look at the host-microbe system as a whole.”
Look closely enough at any plant or animal and you will discover a riot of bacteria, fungi and viruses forming a complex and interconnected ecosystem. A recent explosion of research reveals how deeply we rely on our microbial patterns to keep our bodies functioning, raising profound questions about what it means to be an individual.
Vital functions like digestion and immunity were long assumed to be under the purview of individual organisms, as capabilities developed and were refined through evolution by natural selection — the differential survival and reproduction of individuals. But if our bodies are less an autocracy of identical cells and more a coalition of multitudes, how can we explain their evolution?
Some biologists are calling for a radical upgrade of evolutionary theory, arguing that prevailing ideas, developed from the study of bigger, more easily understood organisms, don’t fit nicely into this new world. Others contend that existing theory just needs to be applied more carefully. All agree that the micro and macro worlds are inescapably interdependent, and that biologists must explore the frontier of their interconnections.
“We have never been individuals,” proclaimed a 2012 paper in The Quarterly Review of Biology by Scott Gilbert, a developmental biologist at Swarthmore College, and his colleagues. This bold assertion echoed previous calls for a reconceptualization of complex organisms as new kinds of individuals — holobionts. The term holobiont encompasses a host animal or plant and all its constituent microbes. All genes within a holobiont, belonging to host or microbes, constitute the “hologenome.”
Holobionts and hologenomes are “incontrovertible realities of nature,” wrote Theis and his colleagues in the journal mSystems. Hologenomes contain vastly more genes than the host genome alone, and since at least a fraction of the microbial genes have significant bearing on the survival and reproduction of the host, we need to consider the hologenome as a possible unit of selection if we want to understand the evolution of the holobiont.
“First and foremost, I think of the holobiont and hologenome as structural definitions,” said Seth Bordenstein, an evolutionary biologist at Vanderbilt University. Along with other researchers, Bordenstein argues that fresh language is needed to refer to this entity, given the ubiquity of host-associated microbes in nature. “We accept the chromosome or the genome as structures. The next level up is the hologenome,” he said.
“The secondary question is: Does the hologenome matter?” he continued. No one knows what proportion of the microbiome will influence host fitness; many are surely just along for the ride. But if there is some degree of cooperation — for instance, if the host provides shelter or nutrients for some microbes that in return metabolize products the host can’t make on its own — then they are more than just two organisms occupying the same space. They are, to a degree, functionally integrated. And that raises the question of whether the hologenome might also matter evolutionarily.
The tighter the integration, the more closely intertwined the fates of host and microbe become. For such holobionts, Bordenstein says, you can’t understand the evolution of either the host genome or the microbial genomes in isolation because the community of organisms as a whole shapes the traits of the individual. “We need to understand what the microbes make, what the host makes and potentially how those products work together,” he said. The holobiont, he argues, adds up to more than the sum of the host and microbes. Out of their interaction emerges a coherent entity that natural selection might act on alongside other units of selection, like the individual or a gene.
Proponents of this hologenomic concept of evolution argue that if there is a fidelity across generations between hosts and microbes, then the holobiont embodies a coming together of numerous, disparate evolutionary lineages into a singular being, a coalition of many that contributes to the functional integrity of the whole. Only when considering the holobiont as a single entity capable of being shaped as a unit by natural selection can we make sense of its complexities.
Variation and Heritability
What might it mean for a holobiont to evolve through natural selection? How can traits emerging from the holobiont as a whole rather than from any individual line of cells in it be “chosen” by nature and spread in the population? The classic recipe for evolution by natural selection begins with a population of individuals with varying characteristics that affect the number of viable offspring they are likely to have. Those characteristics must be inheritable — that is, passed on with some fidelity from generation to generation. A trait could hypothetically double some lucky individual’s lifespan and number of offspring, but unless that trait gets passed on, it’s an evolutionary dead end.
Do holobionts meet those criteria for evolving entities? Microbes and host genomes can interact in ways that profoundly affect host fitness. But whether we inherit our microbiome in something like the way we inherit our genome remains a point of contention.
Parents do pass along microbes to their offspring. For example, females of some species of stink bug nestle a fecal pellet near freshly laid eggs to serve as the larvae’s first meal, thereby inoculating them with their mother’s gut microbiome. Typically, human babies not born by cesarean section acquire their mother’s vaginal microbes en route to the outside world. Mom’s microbes also rub off on a baby through close contact and breastfeeding. Although eventually the microbial community changes as the child moves more freely through the world, these early microbes play an outsize role in immune system development.
Not all of the microbiome is transferred from parent to offspring, but according to Bordenstein, it doesn’t have to be. “Nobody I know expects the microbiome to be inherited in its entirety, faithfully,” said Bordenstein. But if a significant portion of it is, he and others argue that those interactions and their evolution might be understood as a unit of selection.
Poking Holes in Hologenomes
Other researchers think the hologenome concept of evolution stretches the notion of a selectable unit to the point of incoherence. “Just because the microbes are there with one organism at one time does not mean they are a unit of selection, especially if they are not passed on vertically,” said Joan Strassmann, an evolutionary biologist at Washington University in St. Louis who studies microbes.
“I don’t want to make the strong claim that vertical transmission is absolutely necessary, but it’s certainly the most likely mechanism to lead to the cumulative evolution of the partnership as a whole,” said Derek Skillings, a philosopher of biology at the University of Pennsylvania and the City College of New York.
Skillings and other critics argue that there just isn’t enough evidence of vertical transmission of symbionts to allow for the holobiont to be a coherent evolutionary individual. Many of a host’s microbes are acquired from the outside environment, not from its parents. Even when the environment is shared, there is little reason to assume that a parent’s microbes will make it to its offspring. Even if they’re the same sorts of microbes, the direct line of vertical transmission is still necessary to form an evolutionary individual.