Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus

Abstract

Cooperation among individuals is necessary for evolutionary transitions to higher levels of biological organization. In such transitions, groups of individuals at one level (such as single cells) cooperate to form selective units at a higher level (such as multicellular organisms). Though the evolution of cooperation is difficult to observe directly in higher eukaryotes, microorganisms do offer such an opportunity. Here we report the evolution of novel cooperative behaviour in experimental lineages of the bacterium Myxococcus xanthus. Wild-type strains of M. xanthus exhibit socially dependent swarming across soft surfaces by a mechanism known as 'S-motility' that requires the presence of extracellular type IV pili. In lineages of M. xanthus unable to make pili, a new mechanistic basis for cooperative swarming evolved. Evolved swarming is mediated, at least in part, by enhanced production of an extracellular fibril matrix that binds cells-and their evolutionary interests-together. Though costly to individuals, fibril production greatly enhanced population expansion in groups of interconnected cells. These results show that fundamental transitions to primitive cooperation can readily occur in bacteria.

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

“…Velicer and colleagues (Velicer et al 1998(Velicer et al , 2000Velicer & Stredwick 2002;Fiegna & Velicer 2003;Velicer & Yu 2003) and Strassmann and colleagues (Strassmann et al 2000;Foster et al 2002;Fortunato et al 2003a,b;Queller et al 2003) have shown that cheaters may be common in the bacterium Myxococcus xanthus and in the social amoeba, Dictyostelium discoideum, respectively. In these cases, when the organisms are starved they amass into a non-migrating fruiting body or a slug, respectively, and cheater clones make up a small fraction of stalk-like reproductive structures.…”

“…For example, Rainey & Rainey (2003) found that defecting (cheating) genotypes evolved in populations founded by the cooperating type and were fitter in the presence of this type than in its absence. Moreover, Velicer & Yu (2003) demonstrated that micro-organisms can align their evolutionary interests by evolving primitive forms of cooperation. Our findings indicate that traits which potentially benefit the whole population can and do evolve in other contexts, and that an understanding of such evolution may have implications for medically relevant issues such as antibiotic resistance.…”

“…In particular, we wished to examine whether traits that benefit other group members could permit survival of genotypes that otherwise would be eliminated by natural selection, and thereby allow the maintenance of greater genetic variation upon which evolution can operate (Fiegna & Velicer 2003;Velicer & Yu 2003;Greig & Travisano 2004). The maintenance of genetic diversity in microbial communities may be important in the face of changing environmental conditions, such as new antibiotic treatments, and as such, our experimental work may have implications for medical science, as well as evolutionary biology.…”

“…Experimental evidence for the presence or absence of genes coding for group-beneficial traits has been difficult to obtain, in part because investigators often focus on behaviours-such as alarm calling in mammals-whose genetic basis is unknown. Questions surrounding groupbeneficial traits have long plagued behavioural studies in mammalian and other vertebrate systems (Levin 1988;Rainey & Travisano 1998;Sober & Wilson 1998;Bohannan & Lenski 2000;Massey & Peacock 2002;Travisano 2001;Velicer & Yu 2003;West & Buckling 2003;Greig & Travisano 2004). Bacterial models afford the ability to work with large population sizes and rapid generation time so as to provide a system with relative ease of manipulation (Eberhard 1990;Bohannan & Lenski 2000).…”

General Chemotactic Model of Oscillators

“…These elements exhibit not only spatio-temporal patterns but also collective functions. For instance, the cohort migration of mammalian cells forms tissue patterns (15,16), and the Proteus mirabilis effectively invades human urothelial cells by swarming (17). Further, swarm intelligence has been extensively studied in order to enable a collection of simple robots to perform advanced tasks (18).…”