Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Abstract

<jats:p>Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (developmental correction) that arises from density dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.</jats:p>

Artificially selecting bacterial communities using propagule strategies†

“…Looking to the future, and given the considerable challenges of doing these experiments in high throughput (but see Blouin et al 2015), we suggest that simulations such as those performed elsewhere (Williams andLenton 2007, Williams 2007;Xie et al 2019;Doulcier et al 2020) will be very useful to explore different selection regimes, and thus to extract generic conclusions. Such efforts will be critical to develop a theory of artificial selection of microbial communities that can guide the design of new protocols and experiments.…”

“…These challenges of engineering community functions have motivated a surge of interest in evolution-inspired approaches, which treat the community as a unit of selection and explore its ecological landscape in search of consortia with desirable traits (Swenson et al 2000b;Arias-Sánchez et al 2019). This approach has been found to work in silico (Xie et al 2019;Williams 2007;Williams and Lenton 2007;Penn 2003;Doulcier et al 2020) and it has been attempted several times in the laboratory to optimize functions such as toxin removal (Swenson et al 2000a), the manipulation of environmental pH (Swenson et al 2000b), or the modulation of various host traits (Panke-Buisse et al 2015Swenson et al 2000b;Mueller et al 2016;Mueller and Sachs 2015;Gopal and Gupta 2016;Jochum et al 2019). The results of these experimental studies have been mixed (Blouin et al 2015;Arora et al 2019), and it is becoming increasingly clear that the details of how exactly the "offspring" communities are generated from the "parental" communities can be critical for the success of this approach (Raynaud et al 2019;Mueller et al 2016).…”

Spontaneous emergence of multicellular heritability

“…While the emergence of multicellular heritability is widely regarded as a significant challenge in this major evolutionary transition (Doulcier et al 2020;Okasha 2003Okasha , 2013, we show that multicellular heritability may in fact arise spontaneously, as a side-effect of group formation. Our experimental design excludes the possibility of a subsequently-evolved layer of regulation, since the unicellular strains are genetically identical to the multicellular strains, aside from the ace2 deletion.…”

Life history tradeoffs, division of labor and evolutionary transitions in individuality

“…They are rather the result of internal developmental dynamics, i.e., within-collective cellular ecological dynamics (Hammerschmidt et al, 2014;Rose et al, 2020). Selection of developmental mechanisms has long been recognized as an important part of ETIs (Buss, 1987;Michod & Roze, 1997) and can fully be studied by models that explicitly describe the ecological dynamics within collectives (see Ikegami & Hashimoto, 2002;Williams & Lenton, 2007;Xie et al, 2019 for general cell communities; but see Doulcier et al, 2020 for an application to ETIs).…”