Phenological synchrony shapes pathology in host–parasite systems

Abstract

A key challenge surrounding ongoing climate shifts is to identify how they alter species interactions, including those between hosts and parasites. Because transmission often occurs during critical time windows, shifts in the phenology of either taxa can alter the likelihood of interaction or the resulting pathology. We quantified how phenological synchrony between vulnerable stages of an amphibian host ( Pseudacris regilla ) and infection by a pathogenic trematode ( Ribeiroia ondatrae ) determined infection prevalence, parasite load and host pathology. By tracking hosts and parasite infection throughout development between low- and high-elevation regions (San Francisco Bay Area and the Southern Cascades (Mt Lassen)), we found that when phenological synchrony was high (Bay Area), each established parasite incurred a 33% higher probability of causing severe limb malformations relative to areas with less synchrony (Mt Lassen). As a result, hosts in the Bay Area had up to a 50% higher risk of pathology even while controlling for the mean infection load. Our results indicate that host–parasite interactions and the resulting pathology were the joint product of infection load and phenological synchrony, highlighting the sensitivity of disease outcomes to forecasted shifts in climate.

Disease's hidden death toll: Using parasite aggregation patterns to quantify landscape‐level host mortality in a wildlife system

“…First, in addition to amphibian larvae suffering intensity‐dependent parasite mortality (which was the mortality we quantified in this study), infection acquired during the larval stage can lead to severe limb malformations in amphibian metamorphs, which reduce fitness and increase mortality risk (Goodman & Johnson, 2011; Johnson et al., 2002). In amphibian populations in our study area, the prevalence of limb malformation in metamorphs can be as high as 75% and a significant percentage of these malformations have been robustly linked to R. ondatrae infection intensity through laboratory and mesocosm experiments (Johnson et al., 2012, 2013; McDevitt‐Galles et al., 2020). It is therefore likely that the effects of R. ondatrae on amphibian mortality can extend beyond the larval stage.…”

Host phenology can select for multiple stable parasite virulence strategies

“…Many parasite-host systems conform to the assumptions of this model extension such as soil-borne plant pathogens, demicyclic rusts, post-harvest diseases, and many diseases systems infecting univoltine insects. [25][26][27][28] Host phenology drives the timing and prevalence of transmission opportunities for parasites [29][30][31][32][33][34][35][36] which further impacts parasite virulence evolution. 7,8,11,37,38 We add to this body of work by demonstrating that host phenology can also drive bistability in evolutionarily stable parasite strategies.…”

Host phenology can drive the evolution of intermediate virulence strategies in some obligate-killer parasites

“…[12][13][14][15][16][17][18] The phenology of host species also impacts the timing and prevalence of transmission opportunities for parasites which could alter optimal virulence strategies. [19][20][21][22][23][24][25][26] For example, host phenological patterns that extend the time between infection and transmission are expected to select for lower virulence, as observed in some malaria parasites (Plasmodium vivax). In this system, high virulence strains persist in regions where mosquitoes are present year-round while low virulence strains are more common in regions where mosquitoes are nearly absent during the dry season.…”

“…The timing of seasonal activity, or phenology, is an environmental condition affecting all aspects of life cycles, including reproduction, migration, and diapause, in most species (J Anderson et al, 2012;Elzinga and e ae, 2007;Forrest and Miller-Rushing, 2010;Lustenhouwer et al, 2018;Novy et al, 2013;Park, 2019;Pau et al, 2011). The phenology of host species also impacts the timing and prevalence of transmission opportunities for parasites which could alter optimal virulence strategies (Altizer et al, 2006;Biere and Honders, 1996;Gethings et al, 2015;Hamer et al, 2012;MacDonald et al, 2020;Martinez, 2018;McDevitt-Galles et al, 2020;Ogden et al, 2018). For example, host phenological patterns that extend the time between infection and transmission are expected to select for lower virulence, as observed in some malaria parasites (Plasmodium vivax).…”