Survival of the fittest. Nature red in tooth and claw.
The common view of natural selection is based solely on the individual: A trait allows an organism to out-compete its rivals and is thus passed down to its offspring. To suggest otherwise can provoke the ire of certain segments of the scientific community, acknowledged Binghamton University Associate Professor Emerita of Biological Sciences Anne Clark.
But a bibliometric review of 280 scientific studies shows that natural selection can occur on multiple levels of biological organization simultaneously, and not just in social species. Clark is a co-author of the article "Abundant empirical evidence of multilevel selection revealed by a bibliometric review," which recently appeared in the journal Frontiers in Ecology and Evolution.
"The idea of looking at selection at multiple levels is to measure whether a trait is adaptive for individuals within a group," explained Clark, a behavioral ecologist. "And does the frequency or existence of that trait within a group change the way the group functions in comparison with other groups?"
The studies examined by the researchers spanned more than a century, covering everything from viruses to human beings. All attempted to account for multilevel selection (MLS), which provides a broader view of natural selection than individual benefit.
Since 1988, Binghamton University has been a center for foundational work on MLS theory, especially through the research of Professor Emeritus of Biological Sciences David Sloan Wilson and Clark. Review co-author Omar Tonsi Eldakar, now of Nova Southeastern University in Florida, received his PhD at Binghamton in Wilson's lab for his studies of group selection in the wild. In addition to Clark and Eldakar, review co-authors include lead author César Marin, a soil mycorrhizal ecologist; behavioral ecologist Conner Philson; and evolutionary biologist Michael Wade.
Why does multilevel selection remain controversial? Clark pointed to scientific culture. Since the 1960s, key scientists have observed that claims of group benefits weren't subject to rigorous measurement and shouldn't be taken seriously. Some scientists openly banned discussion of group selection in their classrooms, calling it naïve; others claimed that it was exceedingly rare or another term for kin selection.
"If you measure the average increase in the frequency of a trait over generations and then say it's favored by natural selection, you're not wrong," Clark said. "But if I ask you: 'What's the mechanism for the slow increase in that trait over here and the rapid increase over there?' you're not going to be able to tell me. Whereas, if you had looked at different levels, you might see that group competition is more important in one place, or cooperation within groups in another."
Layers of community
So, how does MLS work? Imagine that there are two human tribes. In one, members are solely focused on their individual success. In the other, members are willing to sacrifice themselves for the good of the whole; however, this altruism may cost them time and resources that they could expend on their own children and personal survival.
Which tribe is more likely to survive a crisis, such as an attack from another group? The second. Paradoxically, the willingness for an individual to sacrifice for the group can lead to better survival outcomes. That doesn't mean that everyone in a group will become self-sacrificing, but that groups with self-sacrificing individuals may have a survival advantage, Clark explained.
To take a broader view, individuals not only live in communities but are communities. We are composed of trillions of cells, which comprise our tissues and organs, along with the bacteria in our microbiome and the viruses that afflict us. We live in families, neighborhoods, and countries, as well as ecosystems that bring us into contact with other species.
Every single one of these systems can change over time in response to stimuli, shifting and adapting in response to one another. Groupings can also influence individual success; consider, for example, the case of a family struggling with systemic poverty, or the impact of a troubled neighborhood on the individuals within it.
But it's not just a matter of conscious altruism. In the 1970s, Wade-the final author on the review-conducted seminal research on group selection in flour beetles, a popular "model species" for evolutionary research. Wade created a population of groups, allowed the beetles to reproduce within each group, and selected the smallest or largest groups (in different treatments of the experiment) as "parents" for the next generation of groups. Group size diverged between the two treatments over the generations, demonstrating that group-level selection had occurred. But altruism within groups was not involved; for smaller group sizes, cannibalism of eggs evolved within the group.
Cancer is another interesting example, as are viral illnesses. On one hand, cancer cells no longer cooperate with the rest of the body, subverting the communal good for their individual benefit. But the situation isn't so cut-and-dry.
"In some cases, cancer cells act as a cooperative group in their own right; the ways they spread are strategic," Clark said. "You can also get competition between diseases for host resources."
But what happens within a host is not the whole story; the host's environment is critical, too. If a communicable disease exists in a host population with frequent and predictable contacts, rapid growth with damage to a host may evolve, because this will not stop the host from passing it on. However, such diseases would soon die out in populations of more isolated individuals; in the second scenario, more benign versions would have the advantage, because longer surviving hosts would give the host-and its virus or bacteria-time to find another host. Thus, selection within hosts may favor disease organisms that reproduce faster, but selection between the groups of disease organisms defined by each host may be in the exact opposite direction.
"Multilevel selection complicates the picture because you have to consider all the places where selection could be occurring, and it's possible that selection on one level is headed in a different direction than selection on another level," Clark said.
Real-world applications
There is a real benefit to having a fuller picture of natural selection, particularly in medicine and agriculture. The role that widespread antibiotic use plays in shaping a bacterial arms race is a well-known example.
Another example involves chickens. In one famous study, the agricultural scientist William Muir focused on selecting for egg productivity of hens housed in battery cages. In one experiment, he selected the most productive hen within each cage to breed the next generation of hens (within-group selection). The result? A hyper-aggressive strain of hens that achieved their productivity at the expense of others, resulting in a decline in productivity at the cage level.
In a parallel experiment, Muir selected the most productive cages and used all the hens within the cages to breed the next generation of hens (group-level selection). The result? A docile strain of hens that didn't interfere with each other and achieved a 160% increase in productivity at the cage level in five generations. Based on this and other experiments, group-level selection has become standard practice in animal and plant breeding.
We can also apply the theory to ourselves, keeping Muir's chicken experiments in mind: Are we creating situations that reward competitive or even selfish behaviors? Consider a classroom that grades students on how many questions they ask, penalizing those who are quiet or slow to raise their hands. In that case, the class has selected for rapid responders rather than innovators or deep thinkers, Clark noted.
"We've been encouraged to think about our classroom as a set of diverse individuals. What are we rewarding at the classroom level, and what aren't we rewarding?" she said. "If we looked at different levels, we would understand mechanisms and what's really going on under the hood."
