Social selection within aggregative multicellular development drives morphological evolution

Abstract

Aggregative multicellular development is a social process involving complex forms of cooperation among unicellular organisms. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies and often unfolds within genetically and behaviourally diverse conspecific cellular environments. Here, we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes its 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 cooperator, three cheaters and three antagonists. Fruiting body morphology was found to diversify not only as a function of partner genotype but more broadly as a function of partner social character, with antagonistic partners selecting for greater fruiting body formation than cheaters or the cooperator. Yet even small degrees of genetic divergence between distinct cheater partners sufficed to drive treatment-level morphological divergence. Co-developmental partners also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In summary, we find that even just a few genetic differences affecting developmental and social features can greatly impact 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

“…We quantitatively compared the LPE of fruiting body morphology across MyxoEE-3 populations from both the TS-abiotic and TS-biotic treatment sets and the ancestor (Anc). To do so, we used previously published methods of quantifying four morphological fruiting body traits 11 : three trait medians measured at the resolution of individual fruiting bodies (density, density heterogeneity, and area) and total fruiting body number per assay plate (see Methods: Induction of development and Image acquisition and trait quantification; also ref. 11 ).…”

“…To do so, we used previously published methods of quantifying four morphological fruiting body traits 11 : three trait medians measured at the resolution of individual fruiting bodies (density, density heterogeneity, and area) and total fruiting body number per assay plate (see Methods: Induction of development and Image acquisition and trait quantification; also ref. 11 ). Considering TS-abiotic first, microscopic observation (Fig.…”

“…In Myxococcus literature, sporulation is frequently, if not always, associated positively with fruiting body formation 41 , 96 . While the two developmental processes are indeed often linked, we have recently shown that sporulation can evolutionarily become decoupled from fruiting body development 11 . We observed that MyxoEE-3 treatments that evolved large reductions in morphological-trait values also showed large decreases in sporulation (Fig.…”

“…Fruiting body morphology has diversified strikingly among myxobacterial species (order Myxococcales) 41 , as have many developmental traits already at the intra-specific level among M. xanthus lineages, including fruiting body traits 11 , 68 , 69 , nutrient 70 and cell-density 71 thresholds triggering development, developmental timing 70 and even the genetic elements required for development 72 . However, the relative contributions of various forms of selection and stochastic forces to developmental diversification among myxobacteria remain unclear 41 .…”

“…Forms of selection that may play major roles in diversifying fruiting body morphologies include (i) selection by abiotic or biotic ecological factors on morphological features per se, (ii) selection on non-morphological aspects of development (e.g., 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 73 , substrate stiffness 74 , and social environment 60 , 69 , 75 are known to affect M. xanthus developmental phenotypes, with likely implications for the evolution of fruiting body morphology 11 . The experimental inducibility and facultative character of M. xanthus multicellular development and the versatility for experimental evolution make this bacterium a powerful system for investigating how developmental phenotypes can evolve latently (see definition of “ latent phenotype ” in Methods: Semantics).…”