Persistent trade-offs balance competition and colonization across centuries

Abstract Microbial competition drives rapid adaptation, often forcing organisms to specialize in new ecological niches. Adaptations that improve competitive ability can reduce performance in other environments creating trade-offs. Whether such trade-offs persist in nature—or are eroded as lineages adapt through compensatory changes—remains largely unknown. Here we show that a trade-off between competitive ability and host colonization has been stably maintained in natural Pseudomonas populations for centuries. Wild plant-pathogenic Pseudomonas compete using tailocins—phage-derived molecular weapons that bind to specific cell-surface receptors. Genomic surveys and functional assays reveal that the most broadly lethal tailocins remain rare—while the tailocin’s production increases competitive killing, it also compromises plant colonization. We determine that the polymorphisms behind this trade-off are not transient — historical genomes spanning two centuries show that the trade-off has been maintained for at least 10⁵–10⁶ generations. Our results demonstrate that, in natural populations, a trade-off between competition and pathogenicity is fundamental and not easily overcome. Significance When a microbe colonizes a host, it must both establish infection and outcompete other organisms. Short-term experiments show that gains in competitive ability can reduce colonization, creating trade-offs, but whether microbes resolve these conflicts over long evolutionary timescales is unknown. We show that a trade-off between competitive killing and host colonization has been stably maintained for centuries in natural Pseudomonas populations infecting Arabidopsis thaliana. Tailocins—phage-derived weapons—provide strong competitive advantages, yet their production reduces colonization success, explaining why the most broadly lethal variants remain rare. Genomic surveys and historical genomes spanning two centuries reveal that the polymorphisms underlying this trade-off have persisted across 10⁵-10⁶ generations. Understanding such long-lived constraints can inform antimicrobial strategies that exploit evolutionary trade-offs. Competing Interest Statement The authors have declared no competing interest. Footnotes Classification: Biological Sciences/Evolution ORCID: TB, talia.backman{at}utah.edu JC, jiajun.cui.22{at}ucl.ac.uk EC, emma.caullireau{at}utah.edu EB, u1346590{at}utah.edu IB, ilja.bezrukov{at}tue.mpg.de PG, patricia.girardi{at}utah.edu AH, aubrey.hawks{at}utah.edu JL, lasky{at}psu.edu SL, s.latorre{at}ucl.ac.uk JE, jerberic{at}stanford.edu LL, lua.lopezperez{at}csusb.edu MN, hoelscher.manuela{at}gmail.com AP, allison.perkins{at}utah.edu ES, u6030864{at}umail.utah.edu PA, azadi{at}ccrc.uga.edu MPH, martin.horvath{at}utah.edu AM, muszynski{at}ccrc.uga.edu PL, plang{at}berkeley.edu The new version of this manuscript has updated versions of Figure 1 and Figure 4. Notably, an error in the label of Figure 1B was corrected: the y-label of Figure 1B was inverted.