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Explaining the origin of multicellularity
- Evolution and Development: some insights from Evolutionary Theory

Explaining the origin of multicellularity

The paradox of altruistic behaviour in animal societies was explained by the concepts of kin selection and inclusive fitness (Hamilton 1964). An altruistic gene may invade a population if the sacrifice of one female (males are not considered in demographic analyses) permits the survival of more than two sisters (two sisters will harbour on average one altruistic allele, since the genetic similarity among sisters is 50%). In the case of a multicellular organism, altruism will be easier since all cells share the same genotype. However, the reduction in fitness of a multicellular variant will be more pronounced since, in most cases, many cells fail (renounce) to reproduce.

For example, among Volvocales (phytoflagellates) different related species exist, some remaining unicellular while others build multicellular entities. Under favourable laboratory conditions, a unicellular form will rapidly eliminate a multicellular one, thanks to a higher proliferative capacity accompanied by a low mortality. The picture changes completely if some predator is introduced. Big individuals will be protected by their size while unicellular ones will be eaten and will decrease in number. This simple example illustrates how different species may coexist. It is not possible for a single species to acquire all possible advantages without paying for some inconveniences; otherwise only one species would ultimately survive on earth.

A rapid rate of reproduction favouring the invasive capacity is accompanied by a vulnerability to predation. A big size, on the other hand, may protect from predation and may offer some other advantages, but will imply a longer generation time and a lesser rate of proliferation. More generally any adaptive change in one direction which provides some benefit in terms of fitness, is likely to be accompanied by a cost from another point of view. Evolutionary biologists describe such negative correlations as trade-offs. During the last two decades, major conceptual progresses have been made using the concept of trade-off, for interpreting the diversity of life histories (Charnov 1993, Roff 1992, Stearns 1992). In the extant world, trade-off is the ultimate cause of species coexistence, and it explains why it is possible to be a weed or a tree, a mouse or an elephant. Bacteria have remained very small and quite simple since they appeared more than three billion years ago, but they are still doing very well. Metazoa are much more complex and much bigger. But as stated by all evolutionists, complexity is not an indication of a general tendency toward some progress (Gould 1996). The human species, which may be considered as a summum of complexity is, in other respects, very vulnerable. Multicellularity has certainly been a means for producing a bigger size, thus avoiding predation or becoming a predator. But other interpretations have been considered, for example, a better metabolic utilisation of the environmental conditions (Bonner 2000).

Another problem with multicellularity is that it implies some change at the genetic level. A modification in the genetic program is likely when two cells which arise from a mitosis, remain together and eventually change their phenotypes and their functions. Such changes however do not modify the genome in a permanent way, like mutations. More likely they involve changes in the way genes are regulated by epigenetic processes (Ohlsson et al. 1995, Jablonka and Lamb 1995, Russo et al. 1996, Steele et al. 1998). Cell differentiation, which is a major but still poorly understood issue in developmental biology, is almost exclusively an epigenetic, more or less reversible phenomenon. Theoretical evolutionists now try to understand how such epigenetic changes (sometimes called epimutations) may spread in a population. Much remains to be done in this way of thinking.

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