Travelling with a parasite: the evolution of resistance and dispersal syndromes during experimental range expansion

Abstract

Rapid evolutionary change during range expansions can lead to diverging range core and front populations, with the emergence of dispersal syndromes (coupled responses in dispersal and life-history traits). Besides intraspecific effects, range expansions may be impacted by interspecific interactions such as parasitism. Yet, despite the potentially large impact of parasites imposing additional selective pressures on the host, their role on range expansions remains largely unexplored. Using microcosm populations of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata , we studied experimental range expansions under parasite presence or absence. We found that the interaction of range expansion and parasite treatments affected the evolution of host dispersal syndromes. Namely, front populations showed different associations of population growth parameters and swimming behaviours than core populations, indicating divergent evolution. Parasitism reshaped trait associations, with hosts evolved in the presence of the parasite exhibiting overall increased resistance and reduced dispersal. Nonetheless, when comparing infected range core and front populations, we found a positive association, suggesting joint evolution of resistance and dispersal at the front. We conclude that host–parasite interactions during range expansions can change evolutionary trajectories; this in turn may feedback on the ecological dynamics of the range expansion and parasite epidemics.

A biological invasion modifies the dynamics of a host–parasite arms race

“…Our study reinforces the value of biological invasions as model systems in which to explore rapid evolutionary changes not only in invasive species and the native biota affected by them [10], but also in co-adapted interactions among species [48]. Invasive host-parasite systems are ideal in this respect, because the novel evolutionary pressures engendered by range expansion can result in rapid shifts in adaptive optima for both participants in the arms race [11]. In the case of cane toads in Australia, invasion has produced striking disparities in the ability of co-evolved lungworms to infect their hosts, and in the ability of those hosts to resist infection.…”

“…An absence of native-range parasites (enemy release) in the newly colonized area can facilitate the success of an invasion by allowing individuals of the translocated species to redirect resources from parasite defence into dispersal, growth, reproduction and competitive ability [12,13]. By contrast, high rates of parasitism by native-range or newly encountered parasite taxa can slow an invasion if infection reduces dispersal rate or entails energy allocation for immune defence [11,14].…”

“…Teasing apart the processes that generate these divergent outcomes is challenging in a stable system with coadaptations accumulating over a vast timescale. Biological invasions can provide an opportunity to better understand how parasites and their hosts adapt to each other, and the timescales over which those conflicts are won and lost, because invasions remove the spatial structuring of host and parasite populations and impose novel selective forces on one or both participants [7,10,11].…”

Predicting evolution in experimental range expansions of an aquatic model system

“…This suggests that the increase in equilibrium density might be an emergent property. Indeed, previous work on another ciliate ( Tetrahymena ) shows that evolution in the presence of relatively slowly growing food bacteria can promote more prudent consumption rates ( Fronhofer & Altermatt, 2015 ), thus associating lower maximum population growth rate (selected trait) with higher equilibrium density (emergent trait; see also Zilio et al, 2023 ).…”

“…Recently, experimental evolution and microcosm landscapes have been used to test fundamental predictions and mimic range expansions in the laboratory. Experiments with ciliates ( Fronhofer & Altermatt, 2015 ; Zilio et al, 2023 ), arthropods ( Ochocki & Miller, 2017 ; Petegem et al, 2018 ; Szűcs et al, 2017 ; Weiss-Lehman et al, 2017 ), or plants ( Williams et al, 2016 ) showed the rapid evolution of dispersal and other dispersal-related traits during the experimental range expansions, such as growth, size, locomotory capacity, or exploratory behavior. However, whether we can accurately predict these processes and the accompanying trait evolution from prior information on the genetic or phenotypic characteristics of the expanding populations remains an open question ( Angert et al, 2020 ).…”