I spent the last week of June backpacking in Baxter State Park, Maine. When I finally emerged from the woods, my first stop was Shin Pond Village for a pay shower, a non-rehydrated breakfast, and free internet access. Among the week’s worth of unread emails were a nice surprise and a not-so-nice surprise. The not-so-nice surprise was a manuscript rejected without review; the nice surprise was a new article by Elizabeth Pennisi in Science, which came out when I was somewhere between Upper South Branch Pond and Webster Outlet.

The article, for which I was interviewed before Baxter, synthesizes recent work across a wide range of organisms that suggests that the evolution of multicellularity may not be as difficult a step as we often assume:

The evolutionary histories of some groups of organisms record repeated transitions from single-celled to multicellular forms, suggesting the hurdles could not have been so high. Genetic comparisons between simple multicellular organisms and their single-celled relatives have revealed that much of the molecular equipment needed for cells to band together and coordinate their activities may have been in place well before multicellularity evolved. And clever experiments have shown that in the test tube, single-celled life can evolve the beginnings of multicellularity in just a few hundred generations—an evolutionary instant.

Several examples support the contention that the genetic toolkits for multicellular development were largely present in unicellular ancestors. First, the work of Nicole King and her collaborators on choanoflagellates, the closest living relatives of animals:

Nicole King, a biologist at the University of California (UC), Berkeley, found a revealing window on those ancient transitions: choanoflagellates, a group of living protists that seems on the cusp of making the leap to multicellularity. These single-celled cousins of animals, endowed with a whiplike flagellum and a collar of shorter hairs, resemble the food-filtering “collar” cells that line the channels of sponges. Some choanoflagellates themselves can form spherical colonies. More than 2 decades ago, King learned to culture and study these aquatic creatures, and by 2001 her genetic analyses were starting to raise doubts about the then-current view that the transition to multicellularity was a major genetic leap.

Her lab began turning up gene after gene once thought to be exclusive to complex animals—and seemingly unneeded in a solitary cell. Choanoflagellates have genes for tyrosine kinases, enzymes that, in complex animals, help control the functions of specialized cells, such as insulin secretion in the pancreas. They have cell growth regulators such as p53, a gene notorious for its link to cancer in humans. They even have genes for cadherins and C-type lectins, proteins that help cells stick together, keeping a tissue intact.

All told, by surveying the active genes in 21 choanoflagellate species, King’s group found that these “simple” organisms have some 350 gene families once thought to be exclusive to multicellular animals, they reported on 31 May in eLife.

Volvox also figures importantly in the article:

As cells banded together, they didn’t just put existing genes to new uses. Studies of Volvox, an alga that forms beautiful, flagellated green balls, shows that multicellular organisms also found new ways to use existing functions. Volvox and its relatives span the transition to multicellularity. Whereas Volvox individuals have 500 to 60,000 cells arranged in a hollow sphere, some relatives, such as the Gonium species, have as few as four to 16 cells; others are completely unicellular. By comparing biology and genetics along the continuum from one cell to thousands, biologists are gleaning the requirements for becoming ever more complex. “What this group of algae has taught us is some of the steps involved in the evolution of a multicellular organism,” says Matthew Herron, an evolutionary biologist at the Georgia Institute of Technology in Atlanta.

The steps I mentioned are primarily those outlined by David Kirk in his “12-step” paper:

These studies show that many functions of specialized cells in a complex organism are not new. Instead, features and functions seen in single-celled organisms are rearranged in time and space in their multicellular relatives, says Corina Tarnita, a theoretical biologist at Princeton University. For example, in a unicellular relative of Volvox, Chlamydomonas, organelles called centrioles do double duty. For much of the cell’s lifetime they anchor the two whirling flagella that propel the cell through the water. But when that cell prepares to reproduce, it loses the flagella, and the centrioles move toward the nucleus, where they help pull apart the dividing cell’s chromosomes. Later, the daughter cells each regrow the flagella. Chlamydomonas can both swim and reproduce, but not at the same time.

Multicellular Volvox can do both at once, because its cells have specialized. The smaller cells always have flagella, which sweep nutrients over the Volvox’s surface and help it swim. Larger cells lack flagella and instead use the centrioles full time for cell division.

The idea that differentiated volvocine algae evolved soma because cells can’t swim and divide at the same time is what Vassiliki Koufopanou called the “flagellation-constraint hypothesis.” The importance of flagellar beating for nutrient uptake was confirmed experimentally by my former labmate, Cristian Solari.

Volvox has repurposed other features of the single cell ancestor as well. In Chlamydomonas, an ancient stress response pathway blocks reproduction at night, when photosynthesis shuts down and resources are scarcer. But in Volvox, the same pathway is active all the time in its swimming cells, to keep their reproduction permanently at bay. What was a response to an environmental signal in the single cell ancestor has been co-opted for promoting division of labor in its more complex descendent, [University of Washington biologist Ben] Kerr says.

Dr. Kerr is referring to Aurora Nedelcu’s work, which I have written about before. The article also discusses Will Ratcliff’s evolution experiments with yeast:

As a postdoc working with Michael Travisano at the University of Minnesota in St. Paul, Ratcliff subjected yeast cultures to a form of artificial selection. He allowed only the biggest cells—measured by how fast they settled to the bottom of the flask—to survive and reproduce. Within 2 months, multicellular clusters began to appear, as newly formed daughter cells stuck to their mothers and formed branching structures.

As each culture continued to evolve—some have now been through more than 3000 generations—the snowflakes got bigger, the yeast cells became more durable and more elongated, and a new mode of reproduction evolved. In large snowflake yeast, a few cells along long branches undergo a form of suicide, releasing the cells at the tip to start a new snowflake. The dying cell sacrifices its life so that the group can reproduce. It’s a rudimentary form of cell differentiation, Ratcliff explains.

and our similar experiments with Chlamydomonas:

The yeast results weren’t a fluke. In 2014, Ratcliff and his colleagues applied the same kind of selection for larger cells to Chlamydomonas, the single-celled alga, and again saw colonies quickly emerge. To address criticism that his artificial selection technique was too contrived, he and Herron then repeated the Chlamydomonas experiment with a more natural selective pressure: a population of paramecia that eat Chlamydomonas—and tend to pick off the smaller cells. Again a kind of multicellularity was quick to appear: Within 750 generations—about a year—two of five experimental populations had started to form and reproduce as groups, the team wrote on 12 January in a preprint on bioRxiv.

Ironically, an updated version of that preprint is what was rejected while I was in Baxter. The article also discusses Iñaki Ruiz-Trillo’s work with Capsaspora and Nick Butterfield’s ideas about the role of oxygen (or lack thereof) in the origin of animals, both of which I’m omitting because this is already pretty long. It concludes:

Once organisms had crossed the threshold to multicellularity, they rarely turned back. In many lineages, the number of types of cells and organs continued to grow, and they developed ever-more-sophisticated ways to coordinate their activities. Ratcliff and Eric Libby, a theoretical biologist at Umeå University in Sweden, proposed 4 years ago that a ratcheting effect took over, driving an inexorable increase in complexity. The more specialized and dependent on one another the cells of complex organisms became, the harder it was to revert to a single-cell lifestyle. Evolutionary biologists Guy Cooper and Stuart West at the University of Oxford in the United Kingdom recently confirmed that picture in mathematical simulations. “Division of labor is not a consequence but a driver” of more complex organisms, Cooper and West wrote on 28 May in Nature Ecology & Evolution.

Touched off by the initial transition from one cell to many, a cycle of increasing complexity took hold, and the richness of multicellular life today is the result.

 

Stable links:

Cooper, GA and SA West. 2018. Division of labour and the evolution of extreme specialization. Nature Ecology & Evolution 2: 1161–1167. DOI: 10.1038/s41559-018-0564-9

Herron, MD, JM Borin, JC Boswell, J Walker, I-CK Chen, CA Knox, M Boyd, F Rosenzweig, and WC Ratcliff. 2018. De novo origin of multicellularity in response to predation. bioRxiv DOI: 10.1101/247361

Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. BioEssays 27: 299–310. DOI: 10.1002/bies.20197

Koufopanou, V. 1994. The evolution of soma in the Volvocales. The American Naturalist 143: 907-931. DOI: 10.1086/285639

Libby, E and WC Ratcliff. 2014. Ratcheting the evolution of multicellularity. Science 346:426-427. DOI: 10.1126/science.1262053

Nedelcu, AM and RE Michod. 2006. The evolutionary origin of an altruistic gene. Molecular Biology and Evolution 23: 1460–1464. DOI: 10.1093/molbev/msl016.

Richter, DJ, P Fozouni, M Eisen, and N King. 2018. Gene family innovation, conservation and loss on the animal stem lineage. eLife 7: e34226 DOI: 10.7554/eLife.34226

Solari, CA, S Ganguly, JO Kessler, RE Michod, and RE Goldstein. 2006. Multicellularity and the functional interdependence of motility and molecular transport. Proceedings of the National Academies of Science, USA 103: 1353-1358. DOI: 10.1073/pnas.0503810103