The interplay between host community structure and pathogen life‐history constraints in driving the evolution of host‐range shifts

Abstract

1. The ability of pathogens and parasites to adaptively exploit novel hosts has contributed to their unparalleled diversification along the tree of life. Moreover, evolved host-range shifts are of particular applied interest -for instance, zoonotic 'spillovers' towards humans motivate growing concern about emerging infectious diseases. Thus, identifying the constraints upon, and conditions conducive to, host switching by pathogens is critical to addressing pressing public health and agricultural problems, as well as to understand a major driver of biodiversity.2. How do processes that structure host communities (such as among-host competition) set the selective context for the evolution of pathogen host ranges, and how do these processes interact with trade-offs constraining the evolution of a pathogen's ability to exploit its host?3. Here, we develop a theoretical framework to understand how resource competition among hosts interacts with constraints on pathogen biology in driving host shifts. We characterize how antagonistic pleiotropy in the pathogen's ability to exploit hosts can counteract ecological selection towards host-range shifts.4. We find that although the effects of apparent competition on host-range shifts are mediated through the ancestral pathogen's direct and indirect effects on the entire host community, the effects of exploitative competition on host-range shifts are mediated through exploitative competition's effect on the previously unexploited host.5. Finally, we show that even when changes in host community structure create conditions conducive to host switching, a general trade-off between pathogen virulence and burst size can prevent pathogens from evolving seemingly adaptive patterns of host use. We illustrate how these constraints faced by pathogens shape the ecoevolutionary interaction between pathogen evolution and host communities.6. We discuss how our results inform predictions about the kinds of pathogen lineages likely to exhibit host-range shifts, and the role of apparent versus direct competition in structuring host-pathogen communities over evolutionary time.This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Diversity-disease relationships in natural microscopic nematode communities

“…(13), Panagrolaimus sp. (13), Rhabditella axei (12), Pristionchus entomophagus (10) and Eucephalobus striatus (10) co-occurred at least 10 times with C.…”

“…Remaining variance in community compositions is likely in part attributable to biotic interactions, including nematode-bacteria, nematode-parasite, and nematode-nematode interactions (Okamoto et al 2019;Vandvik et al 2020).Nematode-nematode interactions were examined by searching for specific cooccurrence or exclusion of certain species between samples. Most of the identified nematodes here were either opportunists or part of the basal fauna, although a few species exemplary for progressive succession (~5% of species) were also identified (Ferris et al 2001).…”

“…Remaining variance in community compositions is likely in part attributable to biotic interactions, including nematode-bacteria, nematode-parasite, and nematode-nematode interactions [12,47].…”

“…Interpretation of diversity-disease-correlations has not always been straightforward, as they depend on complex interactions within the natural community. Diversity-disease effects can be obscured or enhanced by parasite encounters, susceptibility and transmission of the species in the community, the order, timeframe and magnitude in which species enter or disappear from the community, life history traits of the host and host range of the parasite [4,[7][8][9][10][11][12][13][14][15][16][17][18][19][20][21]. Interestingly, microscropic species that are relatively easy to grow and manipulate would present excellent models for studying diversity-disease effects, in particular when information from laboratory experiments can be combined with field observations.…”

Interspecific host competition and parasite virulence evolution

“…In addition to effects on total host population density, empirical evidence suggests that interspecific host competition can shift host species frequency ([45,52,53], figure 1 d ). This may affect virulence evolution by determining whether a parasite will adapt to infect one or more host species [54]. In general, populations/communities with multiple host species occurring at similar relative abundances should favour generalists, while those dominated by a single species should favour specialists [55].…”