Evolutionary Constraints in Multicellular Life Cycles: Animals, Plants, and Fungi Compared

While every life cycle eventually passes through a single-celled stage and may have in essence a tabula rasa, this does not mean that the slate is completely blank. The influence of ancestral legacies has been recounted in compelling detail by Buss (1987), which can only be touched on here. A first broad limitation relating to animals stems from their origin in a unicellular protistan flagellate, which imposed a constraint that cells cannot divide while ciliated (related to concurrent need both in mitosis and flagella of the microtubule organizing center; this is recounted in Chap. 4).

Some protists overcame the impasse but the line giving rise to metazoans did not. In turn, some of the early metazoans never did resolve this limitation and abandoned dispersal, but for most lineages the solution was gastrulation. For example, sometimes an early embryonic stage involved a two-layered entity capable of both movement and of further development because ectoderm cells were ciliated whereas the endoderm was not (an analogous example pertains to the motile alga Volvox discussed in Chap. 4).

In other words, one evolutionary solution to the conflict between increasing cell complexity and continued division was resolved by allowing some cells to become elaborated and specialized while retaining others unspecialized, capable of ongoing division, and hence in the creation of germ layers. The synergistic and competitive interactions among these embryonic cell lineages, together with selection operating at the level of the individual, have shaped both early and late ontogeny, the resulting diversity among phyletic blueprints, and ultimately the corresponding life cycles (Buss 1987).

Second, the ancestors of the major multicellular clades (animals, plants, fungi) also began with different starting materials that set the particular boundary conditions and shaped the possible, presenting both evolutionary opportunities and constraints (Buss 1987). The starting condition for animal cells was a flexible membrane boundary, which enabled them to move. Accordingly, the zygote could undergo multiple rounds of division giving rise in ontogeny to differentiated lineages destined for much later positions and varied functions. This, however, rendered animals vulnerable to ‘somatic cell parasites’ that abandoned their regulated somatic role and reverted to uncontrolled mitoses. A counter to this threat is early (within the first few cell divisions of the zygote) germline sequestration.

In its earliest ontogenetic form, this occurs only in animals with the preformistic mode of development; Chap. 5 and Buss 1987, 1985). Such development precludes asexuality because ramet production depends on the presence of a totipotent lineage. Thus, animals have either the capability for cloning at the expense of vulnerability to mutant lineages, or ontogenetic controls that limit such variants at the expense of losing asexuality, but not both.

In sharp contrast to animals, plants have rigid walls and consequently their cells cannot move. Somatic variants, though they still occur, are therefore not a systemic threat. Embryogenesis is not marked by early germline determination. Plants preserve totipotent lineages represented by their various meristems (see Chap. 5) that produce somatic structures and eventually flowers; accordingly, plants have the potential for asexual reproduction. They contend with deviant lineages in unique ways, including stringent selection in the haploid gametophytic phase, noted above (see Chap. 5 and Walbot and Evans 2003). Considerable intercellular communication remains possible in plants via plasmodesmatal channels between adjoining cells.

Fungi, in turn, have certain attributes of both plants and animals. Fungal cell walls are rigid but, unlike plants, septation in the end walls of adjoining hyphal compartments is generally incomplete so they are to varying degrees coenocytic. Certain processes and cytological features such as specialized septa, cell synchrony, balanced dikaryosis, and cellularization at sites of reproduction, regulate systemic mixing. Their largely haploid condition but varied nuclear states involving dikaryosis and heterokaryosis (Chaps. 2 and 5) are related to the exceptional and frequently complex life cycles of fungi, as developed below.