From single cells to multicellular life

All multicellular creatures are descended from single-celled organisms. The leap from unicellularity to multicellularity is possible only if the originally independent cells collaborate. So-called cheating cells that exploit the cooperation of others are considered a major obstacle.

Scientists at the Max Planck Institute for Evolutionary Biology in Plön, Germany, together with researchers from New Zealand and the USA, have observed in real time the evolution of simple self-reproducing groups of cells from previously individual cells.

The nascent organisms are comprised of a single tissue dedicated to acquiring oxygen, but this tissue also generates cells that are the seeds of future generations: a reproductive division of labour. Intriguingly, the cells that serve as a germ line were derived from cheating cells whose destructive effects were tamed by integration into a life cycle that allowed groups to reproduce.

The life cycle turned out to be a spectacular gift to evolution. Rather than working directly on cells, evolution was able to work on a developmental programme that eventually merged cells into a single organism. When this happened groups began to prosper with the once free-living cells coming to work for the good of the whole.

Single bacterial cells of Pseudomonas fluorescens usually live independently of each other. However, some mutations allow cells to produce adhesive glues that cause cells to remain stuck together after cell division. Under appropriate ecological conditions, the cellular assemblies can be favoured by natural selection, despite a cost to individual cells that produce the glues. When Pseudomonas fluorescens is grown in unshaken test tubes the cellular collectives prosper because they form mats at the surface of liquids where the cells gain access to oxygen that is otherwise – in the liquid – unavailable.

Given both costs associated with production of adhesive substances and benefits that accrue to the collective, natural selection is expected to favour types that no longer produce costly glues, but take advantage of the mat to support their own rapid growth. Such types are often referred to as cheats because they take advantage of the community effort while paying none of the costs. Cheats arise in the authors’ experimental populations and bring about collapse of the mats. The mats fail when cheats prosper: cheats obtain an abundance of oxygen, but contribute no glue to keep the mat from disintegrating – the mats eventually break and fall to the bottom where they are starved of oxygen.

Paul Rainey, who led the study at the New Zealand Institute for Advanced Study and the Max Planck Institute for Evolutionary Biology, explains: “Simple cooperating groups – like the mats that interest us – stand as one possible origin of multicellular life, but no sooner do the mats arise, than they fail: the same process that ensures their success – natural selection – , ensures their demise.” But even more problematic is that groups, once extant, must have some means of reproducing themselves, else they are of little evolutionary consequence.

Pondering this problem led Rainey to an ingenious solution. What if cheats could act as seeds – a germ line – for the next set of mats: while cheats destroy the mats, what about the possibility that they might also stand as their saviour? “It’s just a matter of perspective”, argues Rainey. The idea is beautifully simple, but counter-intuitive. Nonetheless, it offers potential solutions to profound problems such as the origins of reproduction, the soma / germ distinction – even the origin of development itself.

In their experiments the researchers compared how two different life cycles affected group (mat) evolution. In the first, the mats were allowed to reproduce via a two-phase life cycle in which mats gave rise to mat offspring via cheater cells that functioned as a kind of germ line. In the second, cheats were purged and mats reproduced by fragmentation. “The viability of the resulting bacterial mats, that is, their biological fitness, improved under both scenarios, provided we allowed mats to compete with each other,” explains Katrin Hammerschmidt of the New Zealand Institute for Advanced Study.

Surprisingly however, the researchers found that when cheats were part of the life cycle, the fitness of cellular collectives decoupled from that of the individual cells: that is, the most fit mats consisted of cells with relatively low individual fitness. “The selfish interests of individual cells in these collectives appear to have been conquered by natural selection working at the level of mats: individual cells ended up working for the common good. The resulting mats were thus more than a casual association of multiple cells. Instead, they developed into a new kind of biological entity – a multicellular organism whose fitness can no longer be explained by the fitness of the individual cells that comprise the collective” says Rainey.

“Life cycles consisting of two phases are surprisingly similar to the life cycles of most multicellular organisms that we know today. It is even possible that germ-line cells, i.e. egg and sperm cells, may have emerged during the course of evolution from such selfish cheating cells,” says Rainey.

Contact

Prof. Dr. Paul Rainey
Max Planck Institute for Evolutionary Biology, Plön

Email: rainey@evolbio.mpg.de

Original publication
Katrin Hammerschmidt, Caroline Rose, Ben Kerr and Paul B. Rainey

Life cycles, fitness decoupling and the evolution of multicellularity

Nature, 6 November 2014; 515, 75-79 (doi:10.1038/nature13884)