Larger Numbers Can Impede Adaptation in Asexual Populations despite Entailing Greater Genetic Variation

Abstract

Periodic bottlenecks play a major role in shaping the adaptive dynamics of natural and laboratory populations of asexual microbes. Here we study how they affect the 'Extent of Adaptation' (EoA), in such populations. EoA, the average fitness gain relative to the ancestor, is the quantity of interest in a large number of microbial experimental-evolution studies which assume that for any given bottleneck size (N0) and number of generations between bottlenecks (g), the harmonic mean size (HM=N0g) will predict the ensuing evolutionary dynamics. However, there are no theoretical or empirical validations for HM being a good predictor of EoA. Using experimentalevolution with Escherichia coli and individual-based simulations, we show that HM fails to predict EoA (i.e., higher N0g does not lead to higher EoA). This is because although higher g allows populations to arrive at superior benefits by entailing increased variation, it also reduces the efficacy of selection, which lowers EoA. We show that EoA can be maximized in evolution experiments by either maximizing N0 and/or minimizing g. We also conjecture that N0/g is a better predictor of EoA than N0g. Our results call for a re-evaluation of the role of population size in predicting fitness trajectories. They also aid in predicting adaptation in asexual populations, which has important evolutionary, epidemiological and economic implications.

Adapting in larger numbers can increase the vulnerability ofEscherichia colipopulations to environmental changes

“…Moreover, the efficiency of natural selection, in favoring beneficial mutations and keeping out deleterious ones, increases with increasing population size (Petit and Barbadilla ; Chavhan et al. ), which is also expected to increase the rate of adaptation. However, little is known about how evolving large asexual populations fare when their environment changes abruptly.…”

“…On the other hand, because natural selection is more efficient in larger populations, it can lead to a rapid increase in the average fitness and severe reduction in the genetic variation of such populations (Desai and Fisher ; Sniegowski and Gerrish ; Chavhan et al. ). Such reduction in variation can potentially be detrimental if the environment changes suddenly, particularly if high fitness in the old environment is correlated with low fitness in the new one (antagonistic pleiotropy sensu Cooper and Lenski (); Cooper ).…”

“…Asexual populations of very different sizes also have markedly different accessibilities to beneficial mutations in identical environments (Wilke ; Desai and Fisher ; Sniegowski and Gerrish ; Chavhan et al. ). This is because beneficial mutations that confer higher fitness gains are generally rarer (Kassen and Bataillon ; Eyre‐Walker and Keightley ; Perfeito et al.…”

Larger bacterial populations evolve heavier fitness trade-offs and undergo greater ecological specialization

“…Using a randomized complete block design (RCBD), we conducted the fitness measurements over six different days, assaying one replicate population of each type in both the environments on a given day (Milliken and Johnson, 2009). We estimated fitness as the maximum growth rate (R) (Kassen, 2014; Ketola and Saarinen, 2015; Vogwill et al , 2016), which was computed as the maximum slope of the growth curve over a moving window of ten readings (Leiby and Marx, 2014; Karve et al , 2015, 2016, 2018; Chavhan et al , 2019a; Chavhan et al , 2019b).…”

“…Population size is known to shape a large variety of evolutionary phenomena and properties, including rate and extent of adaptation (Desai and Fisher, 2007; Desai et al , 2007; Sniegowski and Gerrish, 2010; Chavhan et al , 2019a), repeatability of adaptation (Szendro et al , 2013; Lachapelle et al , 2015), biological complexity (LaBar and Adami, 2016), efficiency of natural selection (Ohta, 1992; Petit and Barbadilla, 2009; Chavhan et al , 2019a), etc. Numerous theoretical and empirical results have indirectly linked population size with the extent of ecological specialization.…”