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

Abstract

Spatial dynamics of range-shifting species can be deeply affected by biotic interactions. One ubiquitous type of biotic interaction involves parasites. These can affect nearly all biological systems and impose major selective pressure on the host, leading to rapid evolutionary responses. Despite the potentially large impact of parasites, their role on host dispersal and subsequent range expansions remains mostly unexplored.Therefore, we investigated whether parasites affect and alter host evolution during experimental range expansions. Using microbial model organisms spreading in microcosm landscapes, we found multi-trait evolution and rapid evolutionary shifts in dispersal syndromes due to spatial dynamics and parasitism. As predicted by theory, hosts that had evolved in the absence of parasites changed their movement pattern and increased dispersal at the range margins. The presence of parasites during the range expansion reshaped host phenotypic divergence between front and core, with hosts exhibiting overall reduced dispersal but increased resistance in the front. We suggest that the evolved differences in resistance and other host traits may be associated with a trade-off between dispersal and foraging efficiency.Our work shows that the eco-evolutionary interactions between host and parasite during range expansions can shift the contenders to novel evolutionary trajectories and result in unexpected evolutionary outcomes. Understanding and finding general patterns to these complex dynamics is of critical relevance for conservation and disease management.

Parasitism and host dispersal plasticity in an aquatic model system

“…We observed reduced swimming speed in the infected groups (Figure 3), which is a frequently observed outcome of parasitic infections (McElroy & Buron, 2014;Binning et al, 2017). In P. caudatum, a negative correlation between speed and dispersal has been previously observed (Zilio et al, 2020). Reduced speed could also have the side effect of reducing predator avoidance.…”

“…Dispersal and dispersal-related traits have a genetic basis, as reviewed extensively by Saastamoinen et al, 2018, and they can rapidly evolve (Phillips et al, 2006;Taylor & Buckling, 2011;Weiss-Lehman et al, 2017;Zilio et al, 2020). However, also plastic responses such as dispersal plasticity have a genetic basis underlined by additive genetic components which could respond to selection (de Jong, 2005;Pigliucci, 2005;Garland & Kelly, 2006;Laitinen & Nikoloski, 2019).…”

“…Adaptive phenotypic plasticity is a powerful solution in many situations (Chevin et al ., 2013; Stamp & Hadfield, 2020), and just like constitutive traits, it has a genetic basis on which selection can act (Pigliucci, 2005; Garland & Kelly, 2006; Laitinen & Nikoloski, 2019). Dispersal-related traits have such a genetic basis (Saastamoinen et al ., 2018) and constitutive dispersal can evolve rapidly in a parasite context (Koskella et al ., 2011; Zilio et al ., 2020). However, the genetics and evolution of dispersal plasticity is less well studied.…”

Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

“…Following the discovery of Holospora bacteria in the 19th century ( Hafkine, 1890 ), there has been extensive research on their morphology, infection life cycle, and taxonomic relationships [for a historical overview, see Fokin and Görtz (2009) ]. More recently, the Paramecium-Holospora system has served as a model to study epidemiology and evolution in experimental microcosms ( Lohse et al, 2006 ; Nidelet et al, 2009 ; Duncan et al, 2011a , 2015 , 2018 ; Castelli et al, 2015 ; Dusi et al, 2015 ; Nørgaard et al, 2020 ; Zilio et al, 2020a , b ).…”

Heritable variation in resistance to the endonuclear parasiteHolospora undulataacross clades ofParamecium caudatum

“…Following the discovery of Holospora bacteria in the 19th century (HAFKINE 1890), there has been extensive research on their morphology, infection life cycle, and taxonomic relationships (for a historical overview, see ). More recently, the Paramecium-Holospora system has served as a model to study epidemiology and evolution in experimental microcosms (LOHSE et al 2006;NIDELET et al 2009;DUNCAN et al 2011a;CASTELLI 2015;DUNCAN et al 2015;DUSI et al 2015;DUNCAN 2018;NØRGAARD 2020;ZILIO 2020b;ZILIO 2020a).…”