Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations

Abstract

Identifying the mechanisms that create and maintain biodiversity is a central challenge in biology. Stable diversification of microbial populations often requires the evolution of differences in resource utilization. Alternatively, coexistence can be maintained by specialization to exploit spatial heterogeneity in the environment. Here, we report spontaneous diversification maintained by a related but distinct mechanism: crowding avoidance. During experimental evolution of laboratory Saccharomyces cerevisiae populations, we observed the repeated appearance of "adherent" (A) lineages able to grow as a dispersed film, in contrast to their crowded "bottomdweller" (B) ancestors. These two types stably coexist because dispersal reduces interference competition for nutrients among kin, at the cost of a slower maximum growth rate. This tradeoff causes the frequencies of the two types to oscillate around equilibrium over the course of repeated cycles of growth, crowding, and dispersal. However, further coevolution of the A and B types can perturb and eventually destroy their coexistence over longer time scales. We introduce a simple mathematical model of this "semistable" coexistence, which explains the interplay between ecological and evolutionary dynamics. Because crowded growth generally limits nutrient access in biofilms, the mechanism we report here may be broadly important in maintaining diversity in these natural environments.experimental evolution | coexistence | fungal adherence | crowding

Hitchhiking and epistasis give rise to cohort dynamics in adapting populations

“…S9 and Dataset S1). We suspect the erg11 mutation is responsible for the plateau because defects in ergosterol biosynthesis (or drug-based inhibition of the pathway) have been shown to result in negative frequency dependence in yeast (35). We observed abnormal well morphology in erg11-containing cultures mirroring the morphology of the "adherent" A-type cells described previously (35).…”

“…Fitness dependence, which can arise through cross-feeding or spatial structuring, often complicates fitness estimates (35)(36)(37)(38)(39). One of our evolved clones (BYS1E03-745) exhibits negative frequency-dependent fitness when competed against an ancestral reference: the clone plateaued at frequency of 0.75 regardless of starting proportion (SI Appendix, Fig.…”

“…We suspect the erg11 mutation is responsible for the plateau because defects in ergosterol biosynthesis (or drug-based inhibition of the pathway) have been shown to result in negative frequency dependence in yeast (35). We observed abnormal well morphology in erg11-containing cultures mirroring the morphology of the "adherent" A-type cells described previously (35). Because our bulk-segregant pool contained random combinations of evolved mutations, both with and without the erg11 mutation, we could successfully quantify the fitness effect of all mutations in this clone with the exception of the erg11 allele itself, which maintained a frequency between 0.8 and 0.9 for the entirety of the 90-generation bulk-segregant fitness assay.…”

The dynamics of molecular evolution over 60,000 generations

“…Instead, their relative abundance can shift by at least ~10-fold during their coexistence. The timing and magnitudes of these shifts vary from population to population; they could reflect ongoing selection on the mechanism of coexistence or a general coupling between the ecologically divergent phenotypes and ordinary fitness gains 28–30 . Further work is needed to distinguish between these scenarios.…”

Evolution in changing environments : heavy metal adaptation in experimental yeast populations as a case study

“…Even experimental conditions that appear homogeneous at first sight often contain different spatial or nutritional niches, and such heterogeneity generally leads to the evolution of diverse specialists, particularly when trade-offs are strong (Rainey and Travisano 1998;Kawecki and Ebert 2004;Le Gac et al 2012;Herron and Doebeli 2013;Traverse et al 2013;Frenkel et al 2015). By contrast, conditions that fluctuate over time select mostly for one generalist type that has the highest geometric mean fitness across all environments (Reboud and Bell 1997;Turner and Elena 2000;Cooper and Lenski 2010), although bet-hedging or increased phenotypic plasticity may also evolve under such circumstances (Levins 1968;Beaumont et al 2009;Leggett et al 2013).…”