Highly complex honeybee communities are one example of phenomena that some scientists think can't be explained by the mainstream theory of evolution alone, but instead by a theory of self-organization.

Courtesy Todd Huffman/Flickr Nearly 150 years after Charles Darwin published On the Origin of Species, evolution has been widely accepted by scientists – and, except for a few religious dogmatic types, the public – as the blueprint for the engine of life.

But not every scientist thinks that evolution as it's now understood and applied is complete. They want to scale it up to the level of populations, even whole ecosystems. Moreover, they say evolution is intertwined with other dynamics that science is just starting to understand.

"The process of evolution is fundamental to the universe. Biology is the most obvious manifestation of it," said Carl Woese, a legendary microbiologist and one of the first proponents of this newly revised evolutionary framework.

Darwin described how changes in an organism are passed from generation to generation, dwindling or spreading through populations depending on their contribution to survival. Biologists later combined this with genetics, which had yet to be discovered in Darwin's time. The fusion – called the modern evolutionary synthesis, or neo-Darwinian evolution – describes evolution as we now know it: Genetic mutations produce changes that sometimes become part of a species' heritage and, when enough changes accumulate, produce new species.

But to Woese and others, change and selection need to be studied at other levels: A honeybee colony, for example, is as much an individual as a single bee. And when explaining how interacting units – bees, or bacteria, or cells – produce the qualities of the whole, change and selection alone might not suffice. What's needed is an understanding of the dynamics of complexity.

"There's nothing wrong with neo-Darwinian evolution in its own right," Woese said, "but it's not large enough to encompass what we know now."

Woese's specialty is bacteria, and he's not afraid of bold theories that turn conventional scientific wisdom on its head. In 1977, he and colleague George Fox rearranged the animal kingdom from five branches into three, two of which comprise microbes.

Microbes make up much of Earth's biomass, and they also cast into relief the shortcomings of neo-Darwinian evolution. A bucket of seawater can contain 60,000 bacterial species, and to Woese, these must be seen as a collective rather than as disparate units.

At the collective level, said Woese, bacteria exhibit patterns of organization and behavior that emerge suddenly, at tipping points of population variation and density called "saltations." Natural selection still favors – or disfavors – the ultimate outcome of these jumps, but the jumps themselves seem to defy explanation solely through genetic changes or individual properties.

Such jumps don't just call into question whether evolution is capable of producing sudden rather than gradual change. That debate raged during the later stages of the last century, but has been largely settled in favor of what paleontologists Niles Eldredge and Stephen Jay Gould termed punctuated equilibrium. By contrast, Woese invokes yet-to-be-quantified rules of complexity and emergence. These, he said, may also explain other exceptional jumps, such as the transition from protein fragments to single cells and from single-celled organisms to multicellular ones.

But even bacterial communities resist framing in isolation. The human body, for example, contains nine bacterial cells for every cell of our own. There's no clear line separating our selves and our bacteria: We're walking ecosystems. The same blurriness exists when considering any collection of interacting organisms.

If these principles seem nebulous in a bacterial context – microbes are, after all, invisible to the eye – then the same principles can be discerned more clearly in the insect world, where some biologists now see certain species, especially honeybees and ants, as forming colonies that should be defined as self-interested organisms unto themselves.

In these so-called superorganisms, individual characteristics – such as the chronologically varying reproductive stages of solitary female bees – lay the foundations for highly complex organizations, such as honeybee hives in which different reproductive stages are assigned to separate worker castes.

According to Arizona State University evolutionary biologist Gro Amdam, until recently, scientists thought the division of labor had a genetic basis, but after scientists sequenced the honeybee genome, they couldn't find a trigger. Hyper-specialization seems to be an emergent property of the collective.

"That's a specific example of how a new pattern can be thrown into play," Amdam said. "You have an ordinary life cycle in an individual, but in a social context it's exploited by the colony."

The superorganism is still shaped by mutation and natural selection, but only recently have biologists, accustomed to thinking of evolution at the individual level, applied the superorganism concept to insects. It may very well have even broader applications.

"Man is the one who's undergoing this incredible evolution now," Woese said. "We see some in the insects, but the social processes by which man is evolving are creating a whole new level of organization."

But as with bacteria and people, how can a sharp distinction be drawn between a honeybee colony and the flowers that both nourish them and rely on them for pollination? And between the flowers and organisms that in turn rely upon them?

"Selection probably happens at all scales, from gene to individual to species to collection of species to ecosystem to we don't even know what," said Maya Paczuski, head of the Complexity Science Group at the University of Calgary.

Paczuski's group sees evolution as taking place at all these levels, with what happens in ecosystems rippling down to individuals, back up to populations, across to other populations, and so on – all simultaneously, and in tandem with the mysterious dynamics of networked complexity.

But does it all happen mechanically? Or does evolution obey some larger imperative?

University of Nevada evolutionary biologist Guy Hoelzer calls that imperative biospheric self-organization. "The idea of evolution is embedded within self-organization," he said. "It coordinates the ecological roles of species so that ecosystems persist and process a great deal of energy."

Woese expanded the concept. "Evolution is a better version of the second law of thermodynamics, of time-zero, which implies that things are going to degenerate until even the atoms fall apart. But maybe that's not the way it's going to play out."

Such theories are still new and controversial. The scientific community at large may never accept them. But ideas do evolve, even Darwin's.

"I think Darwin would be happy as a lark to come back and see what's going on," said Peter Bowler, co-author of Charles Darwin: The Man and His Influence. "He'd say, 'This is quite exciting!'"

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