Cellular differentiation and individuality in the ‘minor’ multicellular taxa

Abstract

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

Geometry shapes evolution of early multicellularity

“…This is found in the germsoma differentiation in multicellular organisms and worker/queen roles in eusocial insects [12][13][14][15][16][17]. While reproductive specialization is not strictly required for division of labor to provide a fitness benefit to the higher-level entity, it has evolved repeatedly in independent lineages [18][19][20][21][22].…”

Organisms or biological individuals? Combining physiological and evolutionary individuality

“…Biological individuality has been a major issue for immunologists since at least the end of the 19 th century (Richet 1894;Richet 1913;Loeb 1930;Loeb 1937;Medawar 1957;Burnet 1962;Hamburger 1978), as emphasized by many historians of the field (Löwy 1991;Moulin 1991;Tauber 1991;Tauber 1994;Löwy 2003). Immunologists have suggested that the immune system is involved in the definition of biological individuality in at least three senses of "individuality" (Pradeu 2012 (Burnet 1962, p. 38-41).…”

“…Leo Loeb shows, in several papers (Loeb 1930;Loeb 1937;Loeb 1953) and in a long book entirely devoted to the topic of biological individuality (Loeb 1945), that there exist degrees of biological difference ("individuality differentials") among individuals, which reflect the uniqueness and unity of each individual, and explain the success or failure of grafts. Medawar, who shared the Nobel Prize with Burnet in 1960 for their work on immune tolerance to grafts, also examines the relation between transplantation and the uniqueness of the individual, an idea further explored by Jean Dausset, who demonstrated the existence of an histocompatibility system in humans (Dausset 1981) (see also (Hamburger 1978)). A striking realization at that time was that biological uniqueness is further reinforced by the fact that even genetically identical individuals have different immune systems (Pradeu 2012).…”

Reproduction, symbiosis, and the eukaryotic cell

“…For example, in the evolution of multicellularity a new kind of reproducing individual arises, but the parts of these individuals (their cells, and also their genes) remain able to reproduce. Systems in which there is a hierarchy of objects in which both parts and wholes reproduce are the source of debates and puzzle cases, because it may be unclear which units are the bearers of fitness (31)(32)(33). Examples include social insects and their colonies, demes and their constituent organisms, and ramets and genets in botany.…”