Stochastic exits from dormancy give rise to heavy‐tailed distributions of descendants in bacterial populations

Abstract

Variance in reproductive success is a major determinant of the degree of genetic drift in a population. While many plants and animals exhibit high variance in their number of progeny, far less is known about these distributions for microorganisms. Here, we used a strain barcoding approach to quantify variability in offspring number among replicate bacterial populations and developed a Bayesian method to infer the distribution of descendants from this variability. We applied our approach to measure the offspring distributions for five strains of bacteria from the genus Streptomyces after germination and growth in a homogenous laboratory environment. The distributions of descendants were heavy‐tailed, with a few cells effectively ‘winning the jackpot’ to become a disproportionately large fraction of the population. This extreme variability in reproductive success largely traced back to initial populations of spores stochastically exiting dormancy, which provided early‐germinating spores with an exponential advantage. In simulations with multiple dormancy cycles, heavy‐tailed distributions of descendants decreased the effective population size by many orders of magnitude and led to allele dynamics differing substantially from classical population genetics models with matching effective population size. Collectively, these results demonstrate that extreme variability in reproductive success can occur even in growth conditions that are far more homogeneous than the natural environment. Thus, extreme variability in reproductive success might be an important factor shaping microbial population dynamics with implications for predicting the fate of beneficial mutations, interpreting sequence variability within populations and explaining variability in infection outcomes across patients.

Wide lag time distributions break a trade-off between reproduction and survival in bacteria

“…S1). Skewed offspring distributions in bacteria were recently documented in other contexts (35) and can strongly affect bacterial population dynamics because they lower the effective population size, amplifying the effect of genetic drift (36).…”

Multiple Merger Genealogies in Outbreaks ofMycobacterium tuberculosis

“…2018 ). It is known that stochastic exit from dormancy can lead to heavy-tailed offspring distributions, with bacteria exiting dormancy earlier having an extremely high reproductive success ( Wright and Vetsigian 2019 ). Also in this case, mathematical modeling will be necessary to investigate whether this mechanism can affect the genealogies of MTB and to identify the coalescent type that would result from such process.…”

Principles of seed banks and the emergence of complexity from dormancy

“…To this end, novel genome-barcoding approaches in combination with Bayesian methods have been used to characterize the variance of reproductive output associated with the resuscitation of dormant bacteria. Such approaches revealed that stochastic resuscitation drawn from a heavy-tailed distribution of variants resulted in a few individuals effectively winning a demographic sweepstake 91 . Not only can these long-range jumps diminish genetic diversity, they can also alter the underlying coalescent structure of a population 92 , 93 .…”