Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

Abstract

Host specificity has a major influence on a parasite's ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world's most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4-10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo-Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hyd. taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host-parasite systems and will provide key insights into parasite invasion potential at regional and global scales.

Climate variation influences host specificity in avian malaria parasites

“…Our findings suggest that variation in the realised host specificity of avian malaria parasites follows a hierarchical process consisting first of heterogeneity in potential host pools (occurring most notably across regions characterised by different precipitation patterns) and evolutionarily conserved host traits or behaviours that limit successful infection (Wells et al . ). Biogeographical structure in host specificity likely reflects prominent roles of vector feeding patterns or shifts in host compositions in response to regional climatic conditions.…”

“…Related models have already been successfully used to uncover global variation in realised host specificity for important zoonotic helminth parasites (Wells et al . ). We have extended the flexibility of these models by incorporating group‐level hyperpriors to capitalise on the added power that partial pooling can provide in mixed effects regressions (Gelman & Hill ).…”

“…Instead, a parasite's local host specificity (herein termed ‘realized host specificity’) can be considered the product of a hierarchical process involving both regional and evolutionary forces (Wells et al . ). For host range expansions to occur, a parasite must first be exposed to a novel host species.…”

“…However, mounting experimental and theoretical evidence suggests that host specificity is not a fixed trait (Poulin & Mouillot 2005;Brooks & Hoberg 2007;Agosta et al 2010;Nylin et al 2018). Instead, a parasite's local host specificity (herein termed 'realized host specificity') can be considered the product of a hierarchical process involving both regional and evolutionary forces (Wells et al 2018b). For host range expansions to occur, a parasite must first be exposed to a novel host species.…”

“…Yet host traits that influence susceptibility, such as clutch size or breeding behaviour, can fluctuate in response to environmental conditions (Møller et al 2013). Despite an accelerated focus on describing host specificity for a multitude of parasites de Vienne et al 2009;Farrell et al 2013;Clark et al 2018;Doña et al 2018;Park et al 2018), few empirical studies recognise this environmental dependency by treating specificity as a geographically labile trait (but see Krasnov et al 2004a,b;Wells et al 2018b).…”