Social selection within aggregative multicellular development drives morphological evolution

Abstract

The evolution of developmental systems might be shaped by both historical differences in developmental features and social selection, among other factors. In aggregative multicellularity, development is itself a social process in which unicellular organisms cooperate in carrying out complex developmental programs. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies. Fruiting body development in myxobacteria often unfolds within genetically and behaviorally diverse conspecific cellular environments that can include social defection and warfare. Here we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners - a benign cooperator, one of three cheaters or one of three antagonists. Fruiting body morphology was found to diversify as a function of developmental partners, revealing adaptation specific to distinct cellular environments. Collectively, antagonistic partners selected for higher levels of robust fruiting body formation than did cheaters or the benign cooperator. Moreover, even small degrees of genetic divergence between the distinct cheater partners were sufficient to drive treatment-level morphological divergence. Co-developmental partners not only shaped mean trait evolution but also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In sum, we find that even few genetic differences affecting developmental and social features can greatly impact the morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.

Hidden paths to endless forms most wonderful: Ecology latently shapes evolution of multicellular development in predatory bacteria

“…In Myxococcus literature, sporulation is frequently, if not always, associated positively with FB formation. While the two developmental processes are indeed often linked, we 37,86 have recently shown that sporulation can evolutionarily become decoupled from fruiting-body development, as occurred during MyxoEE-7 9 . We observed that MyxoEE-3 treatments that evolved large reductions in morphological-trait values also showed large decreases in sporulation (Fig.…”

“…We quantitatively compared LPE of fruiting body (FB) morphology across MyxoEE-3 populations from both the TS-A and TS-B treatment sets and the ancestor (Anc). To do so, we used previously published methods of quantifying four morphological FB traits 9 : three trait medians measured at the resolution of individual FBs (density, density heterogeneity and area) and total FB number per assay plate (see Methods and La Fortezza and Velicer 9 ). Considering TS-A first, microscopic observation (Fig.…”

“…Replicate experimental populations evolving under the same selective pressures often diversify stochastically 87,88 . However, the character of the selective environment can limit the degree of such stochastic diversification, whether for immediately manifested or latent phenotypes 9,29,30,89 . For example, we have recently shown that social selection acting during M. xanthus development can limit the degree of stochastic morphological diversification among evolving populations 9 .…”

“…Fruiting body morphology has diversified strikingly among myxobacterial species (order Myxococcales) 38 , as have many developmental traits already at the intra-specific level among M. xanthus lineages, including fruiting body traits 9,64,65 , nutrient 66 and cell-density 67 thresholds triggering development, developmental timing 66 and even the genetic elements required for development 68 . However, the relative contributions of various forms of selection and stochastic forces to developmental diversification among myxobacteria remain unclear 37 .…”

“…the timing of cell-cell signaling) that may nonetheless impact final fruiting body morphology and iii) selection on non-developmental life-cycle behaviors such as predation and growth-phase motility that pleiotropically impact development. Different biotic and abiotic factors such as nutrient level 69 , substrate stiffness 70 and social environment 56,65,71 are known to affect M. xanthus developmental phenotypes, with likely implications for the evolution of fruiting body morphology 9 . The experimental inducibility and facultative character of M. xanthus multicellular development, and its versatility for experimental evolution, make this bacterium a powerful system for investigating the evolution of latent developmental phenotypes.…”