The Origins of Multicellularity JOHN TYLER BONNER

A R T I C L E S I N T E G R A T I V E B I O L O G Y 27 A R T I C L E S The Origins of Multicellularity JOHN TYLER BONNER There is great interest in the invention of multicellularity because it is one of the major transitions during the course of early evolution.1 Most of the emphasis has been on why it occurred. For instance, recently Gerhart and Kirschner2 have argued that a multicellular organism has gained the advantage of a unicellular ancestor because it can more effectively shield itself from the vagaries of the environment by producing its own internal environment. In broader terms, this is Dawkins’3 argument that a competitively effective way of carrying the genes from one generation to the next is by building a complex soma that safely sees to it that the germ plasm survives. KEY WORDS: multicellularity, cell differentiation, early evolution It has been my contention for some then natural selection will see to it that spectrum. For any one population of an years that while these reasons for the the novelty is retained. I would argue organism there can equally likely be a appearance of multicellularity are con- then that the size increase came first, selection for a size decrease, should vincing, they are achieved at the most and the possible advantages that this there be an open niche for smaller forms. fundamental level by increased size and change might provide would follow. In other words, the direction of the selec- thus the key step is a transition to larger tion for size change depends solely on the size.4–7 Becoming larger makes it pos- I would argue then ecological opportunities, and there is al- sible to be isolated from the outside ways room at the top. When the earth was world and to be able to protect the that the size increase populated with nothing but single cells, genes for the next generation. Further- selection opportunities for multicellular- more, size increase will be accompanied came first, and the ity must have been inexhaustible. by a division of labor in the form of cell Many of the recent discussion of the differentiation, which adds to the selec- possible advantages appearance of multicellularity are con- tive advantages of the organism under fined to animal evolution. It is usually some circumstances. My line of reason- that this change inferred that this was a unique event ing, which will be developed further that did not spawn appreciable diversity presently, is that the first step in the might provide would until the great proliferation of body type evolution of multicellularity was a size in the Precambrian era. This view has increase due to an accident, e.g., a mu- follow. arisen partly because of the fossil record, tation that prevents the daughter cells which is notably sparse until the rich from separating. If the larger cell mass findings in the Burgess Shale and simi- Another well-worn point must be has any advantages, such as ensuring lar deposits. But as someone who was stressed from the outset. One assumes the safety of the germ line by produc- raised as a cryptogamic botanist, it has the reason for the non-stop selection for ing a protected internal environment, always seemed to me that this stress on organisms of increased size is that the animal evolution is rather anthropocen- top of the size scale is an ever-present tric. If one thinks in terms of all organ- open niche, and has been open during isms known to exist today, or to have John Bonner is celebrating his 50th year the entire course of organic evolution. existed in the past, then one can only be in biology at Princeton University. His Among the many lines of evidence to impressed by the diversity of the begin- major research has been in experimen- support this contention, perhaps the nings of multicellularity itself. tal studies on the development of cellu- most compelling is the simple observa- lar slime molds. He also has broad tion that there exists a continuum—a BRIEF DESCRIPTION OF THE interests in various aspects of evolution- complete array of sizes among organ- MAJOR ORIGINS OF ary biology, which had led to a series of isms, from the minutest prokaryotes to MULTICELLULARITY books from Morphogenesis in 1952 to the largest mammals and angiosperms. Sixty Years of Biology in 1996. The only place for further expansion is The danger in describing all the differ- into the unfilled niche at the top of the ent steps toward multicellularity is that the 28 I N T E G R A T I V E B I O L O G Y A R T I C L E S walls and the division products of an asexual spore or a zygote remained glued together. This is well illustrated in the sea lettuce Ulva (Fig. 2) and its smaller relatives, where one can trace the transition from a simple filament to a thickened thallus. A somewhat different mode of becoming multicellular is seen in the Vol- vocales, in which the division products are surrounded and held together by jelly and the colonies they form may be flat, for more often are hollow spheres typified by Volvox, (Fig. 3) the largest member of the group. The Chlorococcales become multicellular in a radically different way. For example, in Pediastrum (Fig. 4) the products of cell division are confined within the mother cell (in a vesicle that Figure 1. lin es th e m oth er cell). While th e daughter cells become detached and swim about using their flagella, they reader could well become overwhelmed did separate examples of aquatic origins are initially imprisoned within the by the detail. My other difficulty is that it is in the form of what is traditionally vesicle and eventually, they lose their a subject I have discussed at some length known as colonies. It is assumed that all a b ility to move, t h ey b ecom e ce- previously.4–8 Here I want to do some- higher plants came from green algae in mented into a flat plate that will burst thing different. To begin, I will adapt one which the cells had moderately rigid free from the vesicle as they grow. of the current molecular phylogenies of the major groups of organisms as pro- posed by Sogin9 (based on a single gene of a small subunit of rRNA), and modify his figure by including only those groups that are multicellular (Fig. 1, Drawings by Hannah Bonner). Thirteen separate in- ventions of multicellularity are indicated in the figure, but this is far below the ac- tual number because some of those eight are well known to be polyphyletic, as I will illustrate. My descriptions will begin with green algae and plants and move clockwise around the figure. The descriptions themselves will be brief, and to make it easier to fix them in one’s mind, some of the more important forays into multicellularity will be accompanied by drawings. The reader may want to skim over this section just suffi- ciently to appreciate the variety of separate ways single cells have evolved into multicellular organisms. Green Algae and Green Plants The green algae began their multicellu- Figure 2. larity in water. They provide some splen- A R T I C L E S I N T E G R A T I V E B I O L O G Y 29 The question why there is such a mentous in nature, and they are to vary- variety of shapes in these algae was ad- ing degrees syncytial or multinucleate, dressed many years ago by Baker,10 who especially in the growth phases of their pointed out that photosynthetic algae life cycle. One very common aspect of did not need to develop an elaborate their multicellularity is that when they feeding mechanism to catch particu- go into their reproductive, or fruiting late food; all they needed was to be phase (Fig. 5), all the nuclei and cyto- able to catch the sun, making it pos- plasm suddenly flow through the hy- sible to invent a great variety of dif- phae to central collection points and ferent shapes, which is exactly what rapidly produce spore-bearing fruiting bodies. These can be quite small, as in they have done. the case of simple molds, or they can be very large mushrooms. Animals In the case of animals, we know little Figure 3. about the transition stages and are left with a huge gap between the sponges and the ancestral single cells. Either all Hydrodictyon is closely related to the known invertebrates, living and fossil, Pediastrum, but differs in that it produces, came from one multicellular ancestor, or by much the same development, a huge possibly there was more than one ances- colony. Finally, I should mention the co- tor, sponges having had a separate origin. enocytic and multinucleate green algae such as Caulerpa, a large marine form Fungi that is attached to the ocean floor by a holdfast. Inside there are no cross-walls, Fungi are a heterogeneous group and but merely a large vacuole surrounded the possibility that they are invented by streaming cytoplasm containing vast multicellularity more than once is a rea- Figure 5. numbers of nuclei. sonable hypothesis. All fungi are fila- Brown Algae and Diatoms The brown algae are largely marine and are notable for having some forms, such as Macrocystis, which are over 100 ft in length.

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