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ARE THE ORIGINS OF ORGANISMAL COMPLEXITY ALSO ROOTED IN NONADAPTIVE PROCESSES?

Multicellularity is widely viewed as a unique attribute of eukaryotes, somehow made possible by the origin of a more complex cellular architecture and, without question, with the assistance of natural selection. However, it is difficult to defend this assertion in any formal way. Complex, multicellularity has only arisen twice, once in animals and once in vascular plants. One might add fungi to the list, although the number of fungal cell types is not large, and there is some question as to whether multicellularity was ancestral to the phylogenetic group that contains animals, fungi, and slime molds. In any event, the probability that two or three origins of multicellularity simply arose by chance within eukaryotes as opposed to prokaryotes is somewhere on the order of 1/4 to 1/2, well below the general standards of statistical validity. Of course, many other eukaryotes are capable of producing a few different cell types, but the same is true for prokaryotes, some of which produce radically different cell morphologies.

Nevertheless, King (2004) states that “this historical predisposition of eukaryotes to the unicellular lifestyle begs the question of what selective advantages might have been conferred by the transition to multicellularity;” and Jacob (1977) argues that “it is natural selection that gives direction to changes, orients chance, and slowly, progressively produces more complex structures, new organs, and new species.” The vast majority of biologists almost certainly agree with such statements. But where is the direct supportive evidence for the assumption that complexity is rooted in adaptive processes? No existing observations support such a claim, and given the massive global dominance of unicellular species over multicellular eukaryotes, both in terms of species richness and numbers of individuals, if there is an advantage of organismal complexity, one can only marvel at the inability of natural selection to promote it. Multicellular species experience reduced population sizes, reduced recombination rates, and increased deleterious mutation rates, all of which diminish the efficiency of selection (Lynch, 2007). It may be no coincidence that such species also have substantially higher extinction rates than do unicellular taxa (Raup, 1978; Stanley, 1985).

Although some aspects of the roots of the cellular interactions that constitute development are likely to reside in the resolution of adaptive conflicts between the advantages of cell–cell cooperation versus going it alone (e.g., Maynard Smith and Szathmáry, 1995; Michod, 1999), it need not follow that natural selection is a sufficient force for the exit from the unicellular world. Many developmental genes previously thought to have originated in the vertebrate lineage, owing to their absence in arthropods and nematodes, are now known to be present in basal lineages of animals



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