Mutualism at the leading edge: Insights into the eco-evolutionary dynamics of host-symbiont communities during range expansion

Abstract

The evolution of mutualism between host and symbiont communities plays an essential role in maintaining ecosystem function and should therefore have a profound effect on their dynamics of range expansion. In particular, the presence of mutualistic symbionts at the leading edge should enhance the propagation of host-symbiont communities. Here we develop a theoretical framework that captures the eco-evolutionary dynamics of resource exchange between hosts and symbionts, and their dispersal dynamics in space. We provide quantitative insights explaining how the evolution of resource exchange may shape community structure during range expansion. Parasitic symbionts receive the same amount of resource from the host as mutualistic symbionts, but at lower cost. This selective advantage is strengthened with resource availability (i.e. with host density), promoting mutualism at the range edges, where host density is low, and parasitism in the population core, where host density is higher. The host growth rate depends on the average benefit provided by the symbiotic community, and is maximal at the range edges where symbionts are more mutualistic. The expansion of host-symbiont communities is pulled by the hosts, but pushed by the symbionts. This spatial selection also influences the speed of spread. In particular, host-symbiont communities with high symbiont density at their core (e.g. resulting from more mutualistic hosts), or at their leading edge (e.g. resulting from symbiont inoculation) spread faster into new territories, and so do hosts with low dependence on their symbionts.

Evolutionary ecology of dispersal in biodiverse spatially structured systems: what is old and what is new?

“…From an evolutionary point of view, dispersing with or without a symbiont is known to be different, and can lead to different dispersal and trait evolutionary trajectories [153,154]. These effects can occur under both mutualistic and parasitic symbioses [155], but parasitic symbioses are also prone to evolve towards manipulation of host dispersal [156,157]. Unfortunately, similarly detailed analyses involving more realistic meta-food webs are missing.…”

Microbiome transfer from native to invasive species may increase invasion risk and shorten invasion lag

“…Although the field of microbial ecology is growing rapidly, the current literature has focused on understanding how the presence or absence of certain microbes may affect host fitness (Fontaine et al, 2022;Kikuchi et al, 2012;Kohl et al, 2014;Fontaine and Kohl, 2020), without explicitly considering the ecological consequences of this fitness advantage. Only few studies have explored the influence of microbiome-related dynamics on multi-species communities (Martignoni et al, 2023(Martignoni et al, , 2020Daybog and Kolodny, 2022), where studies considering how variations in microbial communities may affect invasion have primarily dealt with the transmission of pathogens, rather than with the exchange of mutualistic microbes (Gruber et al, 2019;Faillace et al, 2017). Here we present a theoretical framework to investigate the possibility that microbiome sharing, between and within species, would alter the dynamics of invasion by conferring rapid ecological adaptation to invaders.…”

“…All the codes developed for the manuscript are available on GitHub. The code has been developed by Maria M. Martignoni, 2023, Microbiome transfer code, GitHub repository, at https: //github.com/nanomaria/microbiometransfer.…”