Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease

Abstract

While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome.

Landscape structure drives eco-evolution in host-parasite systems

“…predict spatial epidemiology. Recent work by Jousimo et al (2014) and Höckerstedt et al (2022) support 394 this finding, since the authors show that increased host-gene flow in highly connectivity patches leads to increased resistance, reducing harm to the host, and lower parasite occupancy.…”

“…4). In a host-parasite context we here study an illustrative example of virulence evolution, however, patterns of local adaptation as a result of co-evolution also critically depend on gene flow (Gandon and Michalakis, 2002) within networks (Gibert et al, 2013; Jousimo et al, 2014; Höckerstedt et al, 2022). Beyond host-parasite systems, linking our results to kin selection also implies that landscape structure should modulate the evolution of social behaviour, in general.…”

The first arriving virus shapes within-host viral diversity during natural epidemics

“…lanceolata genotypes to harbour extensive diversity in resistance to powdery mildew Po. plantaginis [ 29 , 93 , 94 ]. This observation, together with our new results, suggests that genotypic variation in resistance in Pl.…”

How do fluctuating ecological dynamics impact the evolution of hosts and parasites?

“…There is now a vast literature of theory on the evolution of hosts and their parasites [1,2]. A wide range of questions about the evolutionary dynamics of hostparasite relationships have been explored, including the nature and role of infection genetics [3][4][5][6][7][8][9][10], the distinction between host tolerance and resistance [11][12][13][14][15][16], the impacts of spatial structure [17][18][19][20][21][22][23][24], the effect of predation [25][26][27][28][29], the impacts of co-infection and superinfection [30][31][32][33][34][35] and more besides. The study of fluctuating dynamics in the host-parasite literature has primarily focused on either epidemiological cycles [36][37][38] or fluctuating selection in the context of host-parasite coevolution (e.g.…”