When Should a Clonal, Modular Organism Divide?

Division has an obvious effect on the birth rate of a clonal organism that suddenly doubles its occurrence in a population. There is, however, a less apparent demographic consequence of clonal multiplication that should not be overlooked. This is the decline in probability of death that follows mathematically as a result of dividing oneself into two physiologically independent individuals instead of continuing to grow as a single entity. As Cook (1979, 1985) has pointed out, the probability of genet extinction is the product of the probabilities of the separate chances of death of the ramets, i.e., the extinction of a genotype becomes up to half as likely if two independent lethal events are necessary.

Thus, an ecological strategy for some species of modular organisms may be to reproduce asexually, or to alternate occasional sexuality with recurring rounds of asexual reproduction. It should be emphasized that in many cases clonal units remain physically associated or within the same neighborhood, in which case mortality events are rarely independent. Also the mathematics assumes that the subdivided units do not suffer a higher individual probability of death than does the parental unit and indeed they may because fission typically is associated with an initial decrease in size and mortality is often size-dependent. Nevertheless, wind-dispersed seeds produced asexually (apomictically), such as occurs in some dandelion populations noted earlier (Janzen 1977b; van Dijk 2013) and the intercontinental movement of microbial clones (Goodwin et al. 1994; Brown and Hovmoller 2002; Gomez-Alpizar et al. 2007; Dutech et al. 2012), are examples of widespread dissemination of ramets. The persistence, size, and vast distribution of such clones imply that they are ecologically successful, at least in the relatively short term (see additional comments in Chaps. 2 and 6).

Thus, speaking generally of modular organisms, we see two trends in life cycles. In aclonal species such as a maple tree, there is concurrence between the genetic and physiological individual, the two in effect coexisting in the same entity. In clonal species, such as the creeping buttercup or a bryozoan, it is adaptive for the two kinds of individual to be separated.

There are also physiological implications of a life history plan that involves either continuous growth as a singular individual or division. As summarized above in Table 5.1, modular organisms characteristically have indeterminate growth. The adjective ‘indeterminate’ has been applied variously in the biological literature; here it will be used following Sebens (1982, p. 209) to mean “the ability to increase and decrease size over a wide range as conditions vary, without an apparent genetically determined upper size limit.” Thus, the size of modular organisms, though ultimately set by mechanical constraints, depends in practice on biotic and abiotic attributes of the local habitat. For instance, it may be imposed in the case of animals by size-selective predators; by refuge size; and by prey abundance and prey quality, or more broadly, energy intake (Sebens 1982). In the case of plants, the factors influencing size include competition for light, water, or inorganic nutrients; pathogens; herbivores; and abiotic assaults from wind storms, lightning strikes, or snow loads.

Clonal, modular organisms can escape some of the allometric consequences of size increase as discussed in Chap. 4. One can hypothesize that as a result of natural selection adult size maximizes individual fitness and test whether growth stops, for example, at an energetically optimal size. This has been a common approach in research on marine sessile benthic invertebrates that are active or passive suspension feeders (Hughes and Hughes 1986; Sebens 1979, 1982, 2002). Such invertebrates include anemones, sponges, hydroids, soft and stony corals, bryozoans, and ascidians (Jackson 1985). Active feeders expend energy to draw water across a feeding surface; passive feeders rely on water currents to move food particles to the organism. In both cases, rates of prey capture depend in part on surface area of the feeding apparatus. These studies take on an additional dimension when the animals are clonal, colonial creatures where the question becomes when (at what size) should a colony divide asexually (McFadden 1986). In essence this tests the broad question of whether modularity can free an organism from metabolic allometry—the advantage of a fragmented genet being more than just in demographic terms.

McFadden (1986) studied particle capture rates in a species of small, alcyonacea soft coral that lives in the lower intertidal zone along the coastline of Western North America. The animal feeds passively by extending its polyps and tentacles to the current; feeding dynamics, particularly as influenced by water velocity, are complex and beyond the scope of this discussion. (Polyps are one body form of members of the Phylum Cnidaria, and each constitutes ‘an individual’. In colonial species, as is the case here, a colony may consist of up to about 100 such feeding polyps, each approximately 6-mm long when fully extended. Tentacles protrude from the polyps and are the prey-capturing surfaces.) This coral is capable of localized movement across hard substrata and occurs as aggregations of colonies, each colony being typically up to about 1.5 cm in diameter, a size maintained by ongoing, endogenously controlled fission. Why are the colonies limited to this size?

Under controlled conditions in laboratory aquaria where particle capture rate could be measured as a function of flow speed and numbers of neighboring conspecific colonies McFadden found that, at all speeds tested, per polyp particle capture rates decreased as colony size increased. This is apparently due to physical interference among the polyps and the declining ratio of peripheral to interior polyps as the circular colony expands. Peripheral polyps are relatively more important than interior polyps at intermediate and higher flow speeds where most particles are trapped because of changes in colony shape accompanying colony expansion. Fission helps maintain a high ratio of peripheral polyps to overall colony area and therefore at first glance it should be best to have the smallest colony possible (recall area:volume relationships in Chap. 4).

However, an increased rate of fission implies having more neighbors, which complicates things. Presence of neighbors decreased the per polyp capture rates of a colony at low water speeds but slightly enhanced capture rates at the highest speed. At low speeds this appears due to depletion of the nutrient flux by upstream colonies, decreased flow velocity, and lower penetration of particles into aggregated colonies. While these factors also play a role at higher speeds, the decreased velocity within an aggregation and reduced deformation of the tentacle crown (and therefore a beneficial reduction in drag forces) by neighbors act to enhance particle capture.

On balance, it appears better to have relatively larger colony size at lower speeds while at intermediate speeds it is advantageous for colonies to divide at a smaller size. Feeding efficiency is maximized at high flow speeds by aggregations of very small colonies. Overall, in terms of feeding efficiency, though it is advantageous for colonies to be as small as possible there is a tradeoff at the point where the neighbor effect diminishes capture rate more than fission enhances it—as McFadden concludes (p. 15) “fission should occur when the decrease in per polyp particle capture rate due to increasing colony size exceeds that due to the presence of neighboring colonies.”

Some caveats apply in interpreting the significance of these specific findings, and are summarized by McFadden (see also Sebens 1979, 1982, 1987, 2002 for general considerations). Beyond these it is worth noting that there are several optimum size models with varying assumptions, for instance about what function is being optimized. In McFadden’s work, the premise is that selection is driving maximization of nutrient intake per unit biomass of the clone, which in turn is assumed to be directly related to growth rate, and ultimately clone size and sexual reproductive potential. More generally, it should be kept in mind that other hypotheses or models based on other selective forces might have produced similar results. Thus, because a model may be in accord with field observations does not mean that it is the correct explanation.

Nevertheless, the energetics postulate provides general testable predictions, which can be further refined and tested should they be borne out in specific situations. Finally, with respect to broader implications of body architecture, Sebens (1982; see also Jackson 1977) makes the following interesting point about indeterminate growth. The size of a solitary indeterminate animal will be set by its shape and the dynamics of energy intake and energetic cost, so growth stops at some energetically optimal, habitat-dependent size.

However, clonal, colonial organisms escape from such energetically imposed size limits by being able to undergo repeated rounds of fission into smaller daughter colonies. In related work, Hughes and Hughes (1986) have shown for the colonial cheilostome bryozoan Electra pilosa that the relationship between metabolic rate and biomass is isometric, i.e., not the negative allometric relationship that normally accompanies volumetric increase. Interestingly, even though zooid production is confined to the colony margin and therefore declines as peripheral area declines relative to volume, the animal compensates partially for this by increasing the budding rate of peripheral zooids and forming a protruding or lobate meristem.

The important point here is that the work described above on optimal feeding with respect to colony architecture in benthic invertebrates surely has relevance to other clonal, modular organisms including microorganisms such as fungi (Andrews 1994). Fungi, of course, do not obtain their nutrients like suspension feeders, but in many cases their colony dynamics, area:volume relationships, and growth patterns on hard substrata are closely analogous. The environmental triggers influencing fungal colony size and morphogenesis, including sporulation, are complex and involve cell density and nutrient depletion, among others (e.g., Chen and Fink 2006; Alkhayyat et al. 2015) and are discussed further with respect to phenotypic plasticity in Chap. 7.