Effect of spatial connectivity on host resistance in a highly fragmented natural pathosystem

Abstract

Both theory and experimental evolution studies predict migration to influence the outcome of antagonistic coevolution between hosts and their parasites, with higher migration rates leading to increased diversity and evolutionary potential. Migration rates are expected to vary in spatially structured natural pathosystems, yet how spatial structure generates variation in coevolutionary trajectories across populations occupying the same landscape has not been tested. Here, we studied the effect of spatial connectivity on host evolutionary potential in a natural pathosystem characterized by a stable Plantago lanceolata host network and a highly dynamic Podosphaera plantaginis parasite metapopulation. We designed a large inoculation experiment to test resistance of five isolated and five well‐connected host populations against sympatric and allopatric pathogen strains, over 4 years. Contrary to our expectations, we did not find consistently higher resistance against sympatric pathogen strains in the well‐connected populations. Instead, host local adaptation varied considerably among populations and through time with greater fluctuations observed in the well‐connected populations. Jointly, our results suggest that in populations where pathogens have successfully established, they have the upper hand in the coevolutionary arms race, but hosts may be better able to respond to pathogen‐imposed selection in the well‐connected than in the isolated populations. Hence, the ongoing and extensive fragmentation of natural habitats may increase vulnerability to diseases.

Soil biota and chemical interactions promote co‐existence in co‐evolved grassland communities

“…We found that plant genotypes interacting with “home” biota showed reduced productivity compared with genotypes within the same community that were exposed to “away” biota. This finding agrees with studies on local adaptation in host–pathogen systems where pathogens tend to be ahead of their hosts in the evolutionary arms race and hence cause more damage to local plants (Höckerstedt et al, ; Kraemer & Boynton, ). As a result, plants can experience below‐ground enemy release and become invasive when introduced to a new continent or as a result of climate‐driven range expansion (Blumenthal, Mitchell, Pyšek, & Jarošík, ; Engelkes et al, ; van Grunsven, van der Putten, Bezemer, Berendse, & Veenendaal, ; Mitchell & Power, ).…”

“…Many studies have documented local adaptation within plant species in response to abiotic properties, such as climate and soil properties (Bischoff et al, ; Brady, Kruckeberg, & Bradshaw, ; Macel et al, ) as well as to co‐occurring plant species, their diversity and chemical signatures (Abakumova, Zobel, Lepik, & Semchenko, ; Grøndahl & Ehlers, ; Thorpe, Aschehoug, Atwater, & Callaway, ). Plants also exhibit local co‐adaptation with microbial species, including mycorrhizal and pathogenic fungi (Höckerstedt, Siren, & Laine, ; Johnson, Wilson, Bowker, Wilson, & Miller, ). While the adaptation of individual species to local environments is well documented, knowledge of how this influences community‐level processes is still lacking.…”

“…Local co‐adaptation with microbial species has most often been recorded in host–pathogen systems (Kraemer & Boynton, ). Fungal pathogens exhibit local adaptation to their host plants such that local plant genotypes tend to experience a more severe infection from local pathogen strains than from pathogens lacking a history of co‐evolution (Crémieux et al, ; Höckerstedt et al, ; Thrall, Burdon, & Bever, ). Plants also show different trajectories of co‐evolution with mycorrhizal fungi on different soil types, with mutualistic interactions between plants and fungi maximized in phosphorus‐deficient soils and parasitic interactions minimized in phosphorus‐rich soils (Johnson et al, ; Pánková, Münzbergová, Rydlová, & Vosátka, ).…”

Agricultural land use disrupts biodiversity mediation of virus infections in wild plant populations

“…However, the pattern we observed suggests that the well‐connected populations are more resistant to pathogen attack, as predicted by spatial co‐evolutionary theory where higher rates of gene flow are predicted to provide the upper hand in the arms race between hosts and their pathogens (Gandon & Michalakis, 2002; Gandon & Nuismer, 2009). Indeed, previous studies in this same network of P. lanceolata populations confirmed disease resistance against the specialist fungal pathogen P. plantaginis to increase with increasing population connectivity (Jousimo et al ., 2014; Höckerstedt et al ., 2018). To date, nothing is known about resistance against viruses in P. lanceolata populations in the Åland Islands.…”

Evolutionary Pathways and Trajectories in Antibiotic Resistance

“…The net result is that, once these "better adapted clones" emerge, they can be maintained even in the absence of antibiotic exposure. Better exploitation of the host's resources generally implies facilitated transmission between hosts, particularly in highly fragmented pathosystems with low connectivity (1068).…”