Earlier I noted that Michael Lynch has doubts about whether natural selection was responsible for the evolution of multicelluarity:
These results, along with our theoretical work on network evolution, challenge the popular idea that modularity arises as a direct consequence of selection for morphological complexity, and by extension raise questions about the common assumption that natural selection was responsible for the emergence of multicellularity.
A couple of years ago, Lynch published a very interesting article entitled, “The frailty of adaptive hypotheses for the origins of organismal complexity” in PNAS (2007) vol. 104, pp. 8597–8604. You can read the article here.
A couple of excerpts relevant to the evolution of multicellularity are below the fold.
The vast majority of biologists engaged in evolutionary studies interpret virtually every aspect of biodiversity in adaptive terms. This narrow view of evolution has become untenable in light of recent observations from genomic sequencing and population genetic theory. Numerous aspects of genomic architecture, gene structure, and developmental pathways are difficult to explain without invoking the nonadaptive forces of genetic drift and mutation. In addition, emergent biological features such as complexity, modularity, and evolvability, all of which are current targets of considerable speculation, may be nothing more than indirect by-products of processes operating at lower levels of organization.
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 (45) 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 (46) 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 (13). It may be no coincidence that such species also have substantially higher extinction rates than do unicellular taxa (47, 48).
Because it deals with observations on historical outcomes, frequently in the face of incomplete information, the field of evolution attracts significantly more speculation than the average area of science. Nevertheless, a substantial body of well tested theory provides the basis for understanding the pathways that are open to evolutionary exploration in various populationgenetic contexts. Four of the major buzzwords in biology today are complexity, modularity, evolvability, and robustness, and it is often claimed that ill-defined mechanisms not previously appreciated by evolutionary biologists must be invoked to explain the existence of emergent properties that putatively enhance the long-term success of extant taxa. This stance is not very different from the intelligent-design philosophy of invoking unknown mechanisms to explain biodiversity. Although those who promote the concept of the adaptive evolution of the above features are by no means intelligent-design advocates, the burden of evidence for invoking an all-powerful guiding hand of natural selection should be no less stringent than one would demand of a creationist. If evolutionary science is to move forward, the standards of the field should be set no lower than in any other area of inquiry.