Factors at multiple scales drive parasite community structure

Abstract

1. Understanding how ecological communities are assembled remains a key goal of ecosystem ecology. Because communities are hierarchical, factors acting at multiple scales can contribute to patterns of community structure. Parasites provide a natural system to explore this idea, as they exist as discrete communities within host individuals, which are themselves part of a community and metacommunity.2. We aimed to understand the relative contribution of multi-scale drivers in parasite community assembly and assess how patterns at one level may mask those occurring at another. Specifically, we wanted to disentangle patterns caused by passive sampling from those determined by ecological drivers, and how these vary with scale.3. We applied a Markov Random Fields model and assessed measures of β-diversity and nestedness for 420 replicate parasite infracommunities (parasite assemblages in host individuals) across two freshwater mussel host species, three sites and two time periods, comparing our results to simulations from four different ecologically relevant null models.4. We showed that β-diversity between sites (explaining 25% of variation in parasite distribution) and host species (41%) is greater than expected, and β-diversity between individual hosts is smaller than expected, even after accounting for parasite prevalence and characteristics of host individuals. Furthermore, parasite communities were significantly less nested than expected once parasite prevalence and host characteristics were both accounted for, but more nested than expected otherwise, suggesting a degree of modularity at the within-host level that is masked if underlying host and parasite characteristics are not taken into account. The Markov Random Fields model provided evidence for possible competitive within-host parasite interactions, providing a mechanism for the observed infracommunity modularity.

Enigmatic freshwater mussel declines could be explained by the biodiversity‐disease relationship

“…Hechinger et al, 2011). In two recent freshwater mussel studies, both positive and negative interactions were recorded between pathogens, including some which appeared to exclude certain parasites from individual mussels (Brian & Aldridge, 2021a, 2023). To our knowledge, these are the only studies to date that considers the community ecology of freshwater mussel parasites, in terms of assembly and interactions.…”

Host and parasite identity interact in scale-dependent fashion to determine parasite community structure

“…Despite recent work in this area (e.g. Devevey et al 2015 ; Rynkiewicz et al 2019 ; Brian and Aldridge 2023 ), our understanding of parasite communities lags behind that of free-living communities (Budischak et al 2016 ).…”

“…The second assumption is that the responses of a single parasite species are consistent across host species for a given factor. A recent example of this assumption comes from Brian and Aldridge ( 2023 ), who studied the response of parasite communities to host- and environment-level factors across two different host mussel species, using joint species distribution models. This approach detected the influence of host size on parasite communities (generally, bigger hosts have more parasites), but could not directly account for the fact that the importance of host size may vary with the different host species.…”

“…between-site, through time, between-host or within-host) is a key consideration when determining the main factors responsible for community assembly and maintenance (Penczykowski et al 2016 ; Bolnick et al 2020a ; Rynkiewicz et al 2019 ; Moss et al 2020 ). The interplay between scales is also important (Johnson et al 2015 ): factors may be important at one scale but not others (Bolnick et al 2020b ), and processes operating at a higher scale may mask those at a lower scale if not properly accounted for (Brian and Aldridge 2023 ). As such, the two assumptions may be challenged at different scales.…”

“…For example, the same parasite species may preferentially target larger hosts of multiple species equally (e.g. Brian and Aldridge 2023 ), but may then be facilitated by a coinfecting parasite in one species and impeded by a coinfector in another, altering community-level transmission (e.g. Mordecai et al 2016 ).…”