Abstract
Organisms harbour myriad microbes which can be parasitic or protective against harm. The costs and benefits resulting from these symbiotic relationships can be context-dependent, but the evolutionary consequences to hosts of these transitions remain unclear.Here, we mapped the Leucobacter genus across 13,715microbiome samples(163studies)to reveal a global distribution as a free-living microbe or a symbiont of animals and plants.We showed that across geographically distant locations(South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes. We further found that multiple Leucobacter sequence variants co-occur in wild Caenorhabditis spp. which combined with natural variation in virulence provides real-world potential for Leucobacter community composition to influence host fitness. We examined this by competing C. elegans genotypes that differed in susceptibility to different Leucobacter species in an evolution experiment. One Leucobacter species was found to be host-protective against another, virulent parasitic species. We tested the impact of host genetic background and Leucobacter community composition on patterns of host-based defence evolution.We found host genotypes conferring defence against the parasitic species were maintained during infection. However, when hosts were protected during coinfection, host-based defences were nearly lost from the population.Overall, our results provide insight into the role of community context in shaping host evolution during symbioses.
Highlights
Microbes can hugely impact the evolutionary biology of their hosts
At the host species level, Leucobacter was found in both C. elegans (22% of samples) and C. ramenei (5% of samples) but not in the three C. briggsae nematodes included in the study
We find that colonisation by multiple Leucobacter amplicon sequence variants” (ASVs) is common, with
Summary
Microbes can hugely impact the evolutionary biology of their hosts. They can cause infectious disease and select for host resistance (Best & Kerr, 2000; Bonneaud et al, 2019; Kerr & Best, 1998; Laine, 2006), be beneficial by providing access to otherwise unobtainable nutrients (Akman et al, 2002; Hosokawa et al, 2010) or confer protection against enemies (Haine, 2008; Jones & Nishiguchi, 2004). By generating novel asymmetries in host competition, symbionts could maintain host genotypes in the population that would otherwise be lost in the absence of symbiosis (Murfin et al, 2019; Park, 1948). Understanding these evolutionary interactions in the ecological noise of wild symbioses remains a challenge given the heterogeneity in both host genetics and microbial symbiont communities. We assessed how host genotype can impact the epidemiology of Leucobacter in terms of certain genotypes super-spreading to more susceptible hosts We discuss how such ecological processes may be linked to observed host evolutionary trends
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