Darwinian selection of host and bacteria supports emergence of Lamarckian-like adaptation of the system as a whole

Abstract

Background: The relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts.

Results: To investigate possibilities for emergent adaptations that may distinguish composite host-microbiome systems from germ-free hosts, we introduce a population genetics model of a host-microbiome system with vertical transmission of bacteria. The host and its bacteria are jointly exposed to a toxic agent, creating a toxic stress that can be alleviated by selection of resistant individuals and by secretion of a detoxification agent ("detox"). We show that toxic exposure in one generation of hosts leads to selection of resistant bacteria, which in turn, increases the toxic tolerance of the host's offspring. Prolonged exposure to toxin over many host generations promotes anadditional form of emergent adaptation due to selection of hosts based on detox produced by their bacterial community as a whole (as opposed to properties of individual bacteria).

Conclusions: These findings show that interactions between pure Darwinian selections of host and its bacteria can give rise to emergent adaptive capabilities, including Lamarckian-like adaptation of the host-microbiome system.

Reviewers: This article was reviewed by Eugene Koonin, Yuri Wolf and Philippe Huneman.

Keywords: Darwinian selection; Emergent adaptation; Holobiont; Host-microbiome interactions; Lamarckian adaptation; Population genetics; Vertical and horizontal transmission.

Fig. 1

Stress-dependent adjustment of bacterial niche size. a, b Short term kinetics of the population-averaged number of bacteria, <N_B >_P (a) and bacterial sensitivity, <x_B >_P (b) for hosts which survived a single pulse of exposure to toxin, T₀ = 5, applied at the initial time step. c Average difference ± standard error (SE) between surviving and non-surviving hosts with respect to the total amount of detox secreted by bacteria over a host generation (shown for each T₀). d Mean carrying capacity for bacteria in the population of hosts, averaged (± SE) over a host generation at different levels of T₀. e Average physiological stress over a host generation, Ŝ _Ph, versus the time average of its carrying capacity for bacteria. Green and red points represent hosts with surviving and non-surviving bacteria, respectively. Blue and orange circles mark population averages for surviving and non-surviving hosts, respectively. Dotted line marks carrying capacity which minimizes the physiological stress. f Same as (e) for the time average of total bacterial detox versus bacterial carrying capacity. Time and population averages are denoted by t and p subscripts, respectively)

Fig. 2

Stress-dependent adaptation within one host generation. a Schematics of the Lamarckian evaluation procedure. b, c The Lamarckian as a function of toxic exposure (b) and bacterial detox coefficient (c). d Bacterial sensitivity and detox per bacteria (inset) as a function of bacterial detox coefficient, after exposure to toxin (T₀ = 5). Shown are time (and population) averages over one generation of unexposed ‘clones’ of surviving parents (orange) and their offspring (blue). e, f Distributions of physiological (Ŝ_Ph) and toxic stress (Ŝ_H), experienced by cloned parents and their offspring, following exposure to a toxin pulse (T₀ = 5), applied at the initial time step. Shown for the case of λ_B = 10^− 4

Fig. 3

Stress-dependent selection of hosts, based on microbiome properties. a Temporal kinetics of active toxin for different initial levels of toxin, T₀. Inset displays the time to neutralize 50% of the toxin. b Temporal kinetics of average detox secretion per bacteria following exposure to toxin at T₀ = 5 (red arrow). λ_B = 10^− 4. Inset reveals an increase of inter-hosts variance in average detox per bacteria. c Kinetics of host population size, N_H, normalized by the host carrying capacity, K_H

Fig. 4

Multi-generational coupling between microbiome properties and host-intrinsic traits. The population of host-microbiome systems was subjected to successive resetting of the active toxin to T = 5, every 5 host generations. a-c Temporal kinetic profiles of average detox per bacteria (a), active toxin (b) and normalized size of the host population (c), with a magnified scale in the inset. Red arrows in (a) mark the start and end of the successive resetting of the toxin. d Inverse correlation between the increase in detox secretion per bacterium and the average toxin resistance (inverse sensitivity) of host, 1/x_H, and bacteria, 1/x_B (inset). Orange overlays correspond to Gaussian filtering of the measured properties