A Complexity Drain on Cells in the Evolution of Multicellularity

Abstract

Abstract. A hypothesis has been advanced recently predicting that, in evolution, as higher-level entities arise from associations of lower-level organisms, and as these entities acquire the ability to feed, reproduce, defend themselves, and so on, the lower-level organisms will tend to lose much of their internal complexity (McShea 2001a). In other words, in hierarchical transitions, there is a drain on numbers of part types at the lower level. One possible rationale is that the transfer of functional demands to the higher level renders many part types at the lower level useless, and thus their loss in evolution is favored by selection for economy. Here, a test is conducted at the cell level, comparing numbers of part types in free-living eukaryotic cells (protists) and the cells of metazoans and land plants. Differences are significant and consistent with the hypothesis, suggesting that tests at other hierarchical levels may be worthwhile. Hierarchical transitions occur when a group of organisms combine to form a higher-level entity (Spencer 1904;Campbell 1958;Simon 1962;Pattee 1970;Eldredge and Salthe 1984;Salthe 1985Salthe , 1993Buss 1987;Bonner 1988;Maynard Smith 1988;Wimsatt 1994;Maynard Smith and Szathmáry 1995;McShea 1996 McShea , 2001bPettersson 1996;Valentine and May 1996;Michod 1999). In the history of life, salient examples include the origin of the eukaryotic cell from symbiotic associations of prokaryotic cells, of multicellular individuals from clones of free-living eukaryotic cells, and of colonies from associations of multicellular individuals. A hypothesis has been advanced recently that predicts that, as such transitions occur, and as the new higher-level entities acquire the ability to feed, reproduce, defend themselves, and so on, their component organisms will tend to lose many of these functional capabilities and therefore will tend to lose many of their internal parts (McShea 2001a). More precisely, the expectation is that the component organisms will tend to lose part types at the next hierarchical level down (Fig. 1). (Technical understandings of the terms part and level will be offered shortly; for present purposes, colloquial meanings suffice.)Concretely, the hypothesis predicts that the cells of multicellular organisms will have fewer part types than freeliving eukaryotic cells, that is, nonparasitic protists (hereafter simply protists; sensu Patterson 1999). At a higher level, in colonial marine invertebrates and social insects, the multicellular individuals (e.g., polyps, zooids) that constitute the more individuated colonies-that is, those in which coloniality is more highly developed (Boardman and Cheetham 1973)-should have fewer part types, on average, than those of their less colonial or solitary relatives (Beklemishev 1969). And at a lower level, the former prokaryotes that today function as organelles in eukaryotic cells (e.g., mitochondria, plastids) should have fewer part types than free-living prokaryotes.Attention to hierarchical level is crucial. A considerable body of e...

The ‘division of labour’ model of eye evolution

“…Blue dots have been added following phalloidin stainings that specifically label the actin filaments of microvilli making up the rhabdomeres. Photograph courtesy of G. Jékely. developed previously and has been referred to as 'complexity drain on cells in the evolution of multicellularity' (McShea 2002).…”

Phylogenetic, Functional, and Geological Perspectives on Complex Multicellularity

“…This perspective reemphasizes a point made earlier by McShea (2002) and others: the evolutionary transition from unicells to complex multicellular organisms has several steps --it is a corridor, not a door. The entrance is marked by genetically mediated, geometrically regular multicellular colonies that derive some fitness benefit from their geometry but pay little penalty for ontogenetic mistakes.…”

Criteria for Conceptual and Operational Notions of Complexity

“…Some researchers have taken precisely this route. Daniel McShea [23,25,24] attempts to determine a number of different indicators of complexity instead of postulating just one way to measure it. He measures aspects such as the number of functional parts of a system, the nestedness of a system, the level of interaction between various hierarchical levels, and so on.…”

“…In the light of this, the article will end with a perhaps unsatisfactory (to some) recommendation: In the absence of a consensus on complexity, the most efficient way forward is to retain complexity as an informal, intuitive concept, while abandoning (at least for the time being) attempts to condense the contradicting ansatzes to a least common denominator. In the context of studying the evolution of complexity this strategy is already, at least partially, followed (see for example [23,24,29]). By giving up the ambition to find a universally accepted concept of complexity now, research efforts can be diverted into empirical studies of the evolution of ''complexity-related'' properties of systems, possibly leading to an emerging understanding of complexity in the future.…”