The evolution of multicellular complexity: the role of relatedness and environmental constraints

Abstract

A major challenge in evolutionary biology has been to explain the variation in multicellularity across the many independently evolved multicellular lineages, from slime moulds to vertebrates. Social evolution theory has highlighted the key role of relatedness in determining multicellular complexity and obligateness; however, there is a need to extend this to a broader perspective incorporating the role of the environment. In this paper, we formally test Bonner's 1998 hypothesis that the environment is crucial in determining the course of multicellular evolution, with aggregative multicellularity evolving more frequently on land and clonal multicellularity more frequently in water. Using a combination of scaling theory and phylogenetic comparative analyses, we describe multicellular organizational complexity across 139 species spanning 14 independent transitions to multicellularity and investigate the role of the environment in determining multicellular group formation and in imposing constraints on multicellular evolution. Our results, showing that the physical environment has impacted the way in which multicellular groups form, highlight that environmental conditions might have affected the major evolutionary transition to obligate multicellularity.

The dimensionality and structure of species trait spaces

“…The degree of organismal complexity, which is related to the diversity of cell types (Valentine et al, 1994), can indeed influence the complexity of species trait space following key functional innovation in multicellular clades (Cox et al, 2021; Knoll, 2011; Sosiak & Barden, 2021). The environment can also be crucial in determining the course of multicellular evolution and organismal complexity, with aggregative multicellularity evolving more frequently on land whereas clonal multicellularity is more frequent in water (Fisher et al, 2020). On the other hand, the number of species and trait characteristics are likely to influence the complexity of species trait spaces beyond the type of organism and the environment (Kohli & Jarzyna, 2021; Zhu et al, 2017).…”

Warm and arid regions of the world are hotspots of superorganism complexity

“…McShea [2], for example, defines complexity as the number of different part types at a given hierarchical level. Within a multicellular organism, phenotypic complexity is most often quantified as the number of cell types [3]. A eusocial insect colony, such as that of ants, bees, wasps and termites, is thought to be analogous to a superorganism with a reproductive queen caste functioning as its germline and non-reproductive worker caste functioning as its soma [4–7].…”

De novoevolution of macroscopic multicellularity

“…Size plays a fundamental role in the evolution of multicellularity, as it allows organisms to explore novel ecological niches (1), affords protection from the external environment (2), and underlies the evolution of cellular differentiation (3)(4)(5)(6)(7). The evolution of macroscopic size has been hypothesized to be a key driver of increased organismal complexity, as large size creates an evolutionary incentive to solve challenges of nutrient and oxygen transportation that are otherwise inescapable consequences of diffusion limitations (8,9).…”