Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Abstract

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting‐edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 90–92%, over the 8–10% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell‐intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non‐senescence, or negative senescence. We end by discussing whether similar levels of non‐genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.

Introduction to: Individual heterogeneity – the causes and consequences of a fundamental biological process

“…The last paper, by Jouvet et al (2018), reports empirical research on neutral heterogeneity. From a quantitative and population genetic perspective, neutral heterogeneity should slow down evolutionary dynamics because it lowers heritability and increases genetic drift (Lande et al 2003).…”

“…Two papers review and develop on the origins and maintenance of individual heterogeneity and its impacts on life-history trajectories (Gangloff et al 2018, Vedder andBouwhuis 2018). The last two contributions illustrate how individual heterogeneity can affect population dynamics and eco-evolutionary interactions within species (Jouvet et al 2018, Smallegange et al 2018, with the contribution from Jouvet et al (2018) focusing on the importance of neutral variation. The special issue ends with some perspectives on the study of individual heterogeneity in ecology and evolution.…”

Integrated population models: powerful methods to embed individual processes in population dynamics models

“…IPMs readily allow for integration of the dynamics and modeling of different sources of heterogeneity. The study of the mechanisms of transmission and generation of individual heterogeneity is an active area of research and a matter of current debate (Bonduriansky and Day 2009, Cam et al 2013, Janeiro et al 2017, Jouvet et al 2018. We need to disentangle the relative roles of genetic effects, parental fixed effects, parental condition, and environmental effects on the transmission of measured and unmeasured individual heterogeneity.…”

The effects of individual nonheritable variation on fitness estimation and coexistence

“…Supported by evidence from bacterial systems (Balaban et al, 2004;Cadena, Fortune, & Flynn, 2017;Gomes et al, 2019;Hashimoto et al, 2016;Jouvet, Rodriguez-Rojas, & Steiner, 2018;Kiviet et al, 2014;Levin, 2004;Trauer et al, 2019), we build two model suites which in later sections will be used to explore how nonheritable variation in fitness components may affect the response of a population under different levels of stress, bias common measures of relative fitness between genotypes or strains and associated selection coefficients, and affect their ability to coexist when placed in competition for shared resources.…”

“…First, we consider bacteria growing under in vitro laboratory conditions with nonheritable variation in cell longevity (elapsed time between cell birth and division) (Hashimoto et al, 2016;Jouvet et al, 2018;Kiviet et al, 2014;Powell, 1958). To facilitate specific arguments to be made about mother and daughter cells, in our models we separate the process of cell division into death of mother cells and birth of daughter cells.…”