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

R M Fisher,J J Boomsma,J Z Shik

doi:10.1098/rspb.2019.2963

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.

Highlights

Macroscopic life on earth has been shaped by the evolution of multicellularity from unicellular ancestors
We found that lineages in aquatic environments were significantly more likely to form multicellular groups through daughter cells remaining attached to mother cells after division (MCMCglmm, difference between aquatic and terrestrial: posterior mode = 5.74, credible intervals (CI) = 2.91 – 9.79, pdiff = 0.0008, Nspecies = 139; figure 2a)
We found that the number of cell types scales allometrically with the total number of cells, and that the specific scaling relationship appears to change as organisms evolved larger body sizes

Summary

Introduction

Macroscopic life on earth has been shaped by the evolution of multicellularity from unicellular ancestors. The objectives of this paper are to (i) describe the variation in multicellular organizational complexity across 139 species by investigating the scaling relationships between body size (total number of cells) and number of cell types; (ii) use phylogenetically controlled comparative analyses across 14 independent multicellular transitions to assess the extent to which the environment determines how multicellular groups form and the consequences for whether obligate multicellularity could evolve; and (iii) test whether constraints imposed by the environment can explain why some lineages have reached higher levels of organizational complexity than others and can account for part of the variation in cell type diversity and differences in scaling relationships

Results

Discussion

32. Schaap P et al 2006 Molecular phylogeny and

Findings

23. Kiss E et al 2019 Comparative genomics reveals the