Marquez-Zacarias, P. | bioRxiv Science

bioRxiv2019

Topological constraints in early multicellularity favor reproductive division of labor

Reproductive division of labor (e.g., germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e., productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e., productivity is a concave function of specialization). Through analytical theory and evolutionary individual based simulations, our work demonstrates that reproductive specialization is strongly favored in sparse networks of cellular interactions, such as trees and filaments, that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization. More broadly, we find that specialization is strongly favored, despite saturating returns on investment, in a wide range of scenarios in which sharing is asymmetric.

evolutionary biology↗

bioRxiv2018

Ecological advantages and evolutionary limitations of aggregative multicellular development

All multicellular organisms develop through one of two basic routes: they either aggregate from free-living cells, creating potentially-chimeric multicellular collectives, or they develop clonally via mother-daughter cellular adhesion. While evolutionary theory makes clear predictions about trade-offs between these developmental modes, these have never been experimentally tested in otherwise genetically-identical organisms. We engineered unicellular bakers yeast (Saccharomyces cerevisiae) to develop either clonally ( snowflake, {Delta}ace2), or aggregatively ( floc, GAL1p::FLO1), and examined their fitness in a fluctuating environment characterized by periods of growth and selection for rapid sedimentation. When cultured independently, aggregation was far superior to clonal development, providing a 35% advantage during growth, and a 2.5-fold advantage during settling selection. Yet when competed directly, clonally-developing snowflake yeast rapidly displaced aggregative floc. This was due to unexpected social exploitation: snowflake yeast, which do not produce adhesive FLO1, nonetheless become incorporated into flocs at a higher frequency than floc cells themselves. Populations of chimeric clusters settle much faster than floc alone, providing snowflake yeast with a fitness advantage during competition. Mathematical modeling suggests that such developmental cheating may be difficult to circumvent; hypothetical choosy floc that avoid exploitation by maintaining clonality pay an ecological cost when rare, often leading to their extinction. Our results highlight the conflict at the heart of aggregative development: non-specific cellular binding provides a strong ecological advantage - the ability to quickly form groups - but this very feature leads to its exploitation.

evolutionary biology↗