Social hosts evade predation but have deadlier parasites

Abstract

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite: parasite virulence evolves to balance these costs and benefits. Predators can in theory shift this balance by consuming hosts. However, the non-consumptive effects of predators may be as important as their consumptive effects. Here, we use an eco-coevolutionary model to show that predators select for host grouping, a common anti-predator, defensive social behaviour. Host grouping simultaneously increases parasite transmission, thus within-host parasite competition, and therefore favours more exploitative, virulent, parasites. When parametrized with data from the guppy-Gyrodactylus spp. system, including our experimentally demonstrated trade-off between virulence and transmission, our model accurately predicted the common garden-assayed virulence of 18 parasite lines collected from four Trinidadian guppy populations under different predation regimes. The quantitative match between theory and data lends credence to the model insight that the non-consumptive, social behaviour pathway is entirely responsible for the observed increase in virulence with predation pressure. Our results indicate that parasites play an important, underappreciated role in guppy evolutionary ecology. Moreover, group living is a common anti-predator defence and our general model accommodates host-parasite interactions across taxa: its insight into the interactions among predation, sociality, and virulence evolution may apply broadly. Our results additionally suggest that social distancing, by reducing host-host contact, can select for less virulent parasites and pathogens.

Parasite gene flow in riverine habitats: ascertaining the roles of stream drift, river bifurcations and host dispersal

“…Renifer aniarum individuals collected from the Freese Dam site were consistently diverged from all other sampling locations independent of geographic distance. It is of note that this same pattern of population subdivision associated with the reservoir was also found for the recently delisted host, N. harteri paucimaculata, whose post-delisting monitoring was conducted concurrently with this study (Janecka et al 2021). We do not have a current biological explanation for the concordance of the results for both this host and the parasite, however two organisms whose data independently identifies the same pattern warrants further consideration.…”

“…Parasites are an integral and ubiquitous facet of river ecosystems. Infection from parasites with riverine or partially riverine life-cycles exact high costs to free-living hosts and can impose alterations to host reproduction, behavior and survival (Anderson & May 1979;Marcogliese & Pietrock 2011;Walsman et al 2021). Riverine parasites also cause significant morbidity and mortality to fish of conservation (Lymbery et al 2020) and commercial concern (Krkosek et al 2007).…”

“…Renifer aniarum infects the entire water snake community of the Colorado and Concho Rivers: Nerodia erythrogaster, N. rhombifer and N. paucimaculata (Janecka et al in prep). The population structure for two of the snake species has been examined: Janecka et al (2021) found isolation by distance and population subdivision in N. paucimatuala, while Rodriguez et al (2012) found no population subdivision for N. erythrogaster among the three reaches of the river. The parasite's use of multiple snake species, especially where one shows no genetic structure among the sampled region, may facilitate its dispersal up stream and across branches of the river and thereby, eliminate or reduce the influence of stream drift and DEN on its population structure.…”

Predation shifts coevolution toward higher host contact rate and parasite virulence

“…All code required for the analyses and figures is provided as electronic supplementary material [52].…”

Skin bacterial microbiome diversity predicts lower activity levels in female, but not male, guppies,Poecilia reticulata

“…Both male [40] and female [41,42] guppies prefer more active mates. Similarly, host grouping behaviour, such as shoaling in guppies, has fitness benefits, including access to mates, foraging efficiency and defence against predators [43–47]. Therefore, guppies are an ideal system with which to test whether the skin microbiome is associated with fitness-relevant behaviours.…”