One Equals Many: A New Take on Evolution

Looks someone needs some new microbes...
On the left is an example of a healthy coral, on the right an example of bleaching. Photo courtesy NOAA.

By: Sara Knight
BU News Service

When English poet John Donne claimed that “no man is an island,” he probably did not anticipate how closely his philosophical musings would align with biological theory four centuries later. As genetic research progresses, scientists are realizing that evolution may be more about cooperation among organisms than competition – truly, no organism is an island unto itself.

Biologists increasingly can pinpoint instances of interdependence among species in all kingdoms of life – leading some to believe it is time for traditional Darwinian theory to evolve. Mounting evidence of cooperation among diverse creatures and their respective microbial communities provides tantalizing hints of a more comprehensive view of life – one that challenges the definition of an organism. For decades many microbiologists have believed that no organism evolves alone, but rather as a joint effort with the millions of microscopic creatures teeming with them – fungal, bacterial, and protist. Now, evolutionary biologists are catching on: some think that natural selection acts on “super organisms,” the creature plus its microbes, rather than an organism itself.

Charles Darwin proposed the theory of natural selection in 1859, and it remains a hallmark of evolutionary biology today. Natural selection’s basic tenet is that traits that prove beneficial to an organism will become more common over successive generations. While this basic premise seems almost obvious in its simplicity, many evolutionary puzzles are left unaddressed. For example, the level of organization on which natural selection acts remained an enigma. Do evolutionary pressures act on cells themselves, or whole organisms… or even groups of organisms?

Biologists Eugene Rosenberg and Ilana Zilber-Rosenberg think they have the answer. In 2007 they proposed that organisms adapt to their environments with and because of their microbial communities. They noted that a change in the makeup of species in Mediterranean corals’ microbe population, prompted by changing sea temperatures, enabled the coral to fight off a devastating bleaching virus. The coral, which lacks an adaptive immune system, overcame a viral threat in one generation. The microbial community of the coral successfully fought off the lethal threat, ensuring its survival into another generation. Their observation led the team to develop the hypothesis that natural selection acts not just on one set of genes, but on all of the genes within (and on) an individual, including those of the micro-occupants.

Painting detail from Georges Seurat’s “La Parade de Cirque.”
Are we more than the sum of our parts?

All lifeforms possess robust microbial communities that are linked to physiologic function – humans, for example, rely on hundreds of species within our gut to digest our food and absorb nutrients. Hyenas have unique microbe collections in their anal glands, the distinctive scent of which acts as a badge of pack membership. The mixture of intestinal microbes in the common fruit fly influences with whom they choose to mate. Rosenberg believes these facts justify extending his team’s hypothesis to encompass all life, rather than just this specific Mediterranean coral.

Biologists have long accepted the importance of microbes to the lives of larger creatures – for example, the mitochondria in your own cells originated from a once free-living bacterium that was engulfed by a larger cell – yet many hesitate to agree with Rosenberg’s broad generalization of cooperative evolution in larger creatures.

Roberto Iglesias Prieto of the National Autonomous University of Mexico does not believe Rosenberg and his team proved that the Mediterranean coral was suffering from the viral perpetrator they identified. He, among other marine biologists, calls for a more rigorous examination of Rosenberg’s claim. Iglesias Prieto also cautions that an organism’s fitness might not rely on its entire set of microorganisms, but probably only its beneficial microbes.

Other biologists like John R. Finnerty, director of Boston University’s marine program echo this caveat. Finnerty does not question Rosenberg’s basic claim, but suggests the primary coral research does not support the larger hypothesis that natural selection acts on super-organisms. In some cases, a creature may need a very specific species of microbe to fill a role, while in others the co-occupancy is more of an incidental arrangement between the microbe and host, Finnerty says. The relationship between host and microbe can be very flexible – a fact that Rosenberg’s hypothesis does not address.

Despite these concerns, biologists are becoming more interested in the role our resident microbes fill. In 1998 microbiologist Lynn Margulis wrote that “the full impact of the symbiotic view of evolution has yet to be felt.” Her foresight anticipated Rosenberg’s ambitious, broadened concept of how to define an organism and a concept of evolution that stresses cooperation, rather than competition, as the main catalyst for change. Researchers are currently working toward teasing out the exact roles microbes play in the production of life, but there is a general-consensus that we literally are more than the sum of our parts.

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