Parasite metacommunities: Evaluating the roles of host community composition and environmental gradients in structuring symbiont communities within amphibians

Abstract

Ecologists increasingly report the structures of metacommunities for free-living species, yet far less is known about the composition of symbiont communities through space and time. Understanding the drivers of symbiont community patterns has implications ranging from emerging infectious disease to managing host microbiomes. Using symbiont communities from amphibian hosts sampled from wetlands of California, USA, we quantified the effects of spatial structure, habitat filtering and host community components on symbiont occupancy and overall metacommunity structure. We built upon a statistical method to describe metacommunity structure that accounts for imperfect detection in survey data-detection error-corrected elements of metacommunity structure-by adding an analysis to identify covariates of community turnover. We applied our model to a metacommunity of eight parasite taxa observed in 3,571 Pacific chorus frogs (Pseudacris regilla) surveyed from 174 wetlands over 5 years. Symbiont metacommunity structure varied across years, showing nested structure in 3 years and random structure in 2 years. Species turnover was most consistently influenced by spatial and host community components. Occupancy generally increased in more southeastern wetlands, and snail (intermediate host) community composition had strong effects on most symbiont taxa. We have used sophisticated but accessible statistical methods to reveal that spatial components-which influence colonization-and host community composition-which mediates transmission-both drive symbiont community composition in this system. These methods allow us to associate broad patterns of community turnover to local, species-level effects, ultimately improving our understanding of spatial community dynamics.

Tracking the assembly of nested parasite communities: Using β‐diversity to understand variation in parasite richness and composition over time and scale

“…For example, the only two ponds that lacked a common trematode parasite ( Cephalogonimus americanus ) were also the only ponds with American bullfrog ( Rana catesbeiana ) larvae, which are a less competent host that could reduce C. americanus abundance (Johnson et al, 2013). Consequently, the host community could represent one possible selection mechanism driving parasite community composition, as previously reported in similar studies (Johnson et al, 2013; Krasnov, Shenbrot, Mouillot, Khokhlova, & Poulin, 2005; Maestri, Shenbrot, & Krasnov, 2017; Mihaljevic, Hoye, & Johnson, 2017). More broadly, our results are consistent with a large body of work indicating that ecological selection can strongly structure parasite communities across localities (e.g.…”

Eutrophication, biodiversity loss, and species invasions modify the relationship between host and parasite richness during host community assembly

“…For parasites, transmission is the combination of dispersal and establishment, so multiple parasite species in a host population or community function as a metacommunity connected via transmission among host individuals (Borer, Laine, & Seabloom, 2016;Kuris, Blaustein, & Alio, 1980;Mihaljevic, 2012;Mihaljevic, Hoye, & Johnson, 2018;Sousa, 1994). As such, metacommunity theory can be used to generate predictions about the relationship between host and parasite richness.…”

Animal host–microbe interactions

“…David et al., ; Kurilshikov, Wijmenga, Fu, & Zhernakova, ), a key theme was testing for effects of local environment, diet or host genetic background on symbiont community composition, either between populations of a single species (Kohl, Varner, Wilkening, & Dearing, ; Näpflin & Schmid‐Hempel, ) or between cohabiting species (Muletz Wolz, Yarwood, Campbell Grant, Fleischer, & Lips, ). Mihaljevic, Hoye, and Johnson () extended this to also consider the role of alternate host species, in conjunction with environmental factors, in shaping symbiont communities across populations of a focal host species. Within a host species, the spatial and hierarchical structure of social interactions was also shown to shape the transmission of individual microbes (and disease susceptibility) in populations (Keiser, Pinter‐Wollman, Ziemba, Kothamasu, & Pruitt, ; Keiser et al., ; Raulo, ), as were several different types of indirect interactions.…”

“…These processes also aid in understanding the scaling relationships and feedback loops occurring across multiple levels of biological organisation (within‐host dynamics, among‐host dynamics, across host community dynamics). Extensions of metacommunity theory, modified for organisms living on or in eukaryotic hosts (Mihaljevic et al., ), may be particularly useful in addressing these questions. Likewise, unravelling the impact of microbiota on host physiology, behaviour and population dynamics, particularly in the context of environmental stressors, are key issues for future research.…”