How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale?

Abstract

Social interactions with conspecifics are key to the fitness of most animals and, through the transmission opportunities they provide, are also key to the fitness of their parasites. As a result, research to date has largely focused on the role of host social behavior in imposing selection on parasites, particularly their virulence and transmission phenotypes. However, host social behavior also influences the distribution of parasites among hosts, with implications for their evolution through non-random mating, gene flow, and genetic drift, and thus ability to respond to that selection. Here, we review the paucity of empirical studies on parasites, and draw from empirical studies of free-living organisms and population genetic theory to propose several mechanisms by which host social behavior potentially drives parasite evolution through these less-well studied mechanisms. We focus on the guppy host and Gyrodactylus (Monogenea) ectoparasitic flatworm system and follow a spatially hierarchical outline to highlight that social behavior varies between individuals, and between host populations across the landscape, generating a mosaic of ecological and evolutionary outcomes for their infecting parasites. We argue that the guppy-Gyrodactylus system presents a unique opportunity to address this fundamental knowledge gap in our understanding of the connection between host social behavior and parasite evolution. Individual differences in host social behavior generates fine-scale changes in the spatial distribution of parasite genotypes, shape the size, and diversity of their infecting parasite populations and may generate non-random mating on, and non-random transmission between hosts. While at population and metapopulation level, variation in host social behavior interacts with landscape structure to affect parasite gene flow, effective population size, and genetic drift to alter the coevolutionary potential of local adaptation. Significance statementSocial interactions between animals shape the evolution of the pathogens that infect them. Most research exploring this phenomenon has focused on the selection such interactions impose, but social hosts also shape parasite evolution by determining the ability of their parasites to respond to that selection. Here, we explore how host social behavior drives parasite evolution by shaping non-random mating, gene flow, and genetic drift, from the scale of the individual to the landscape. The relative strength of these evolutionary mechanisms can have striking implications for the evolution of parasite traits such as virulence and alter the evolutionary trajectories of populations across the landscape. We emphasize the importance of studies combining parasite population genetics, host social behavior, and landscape processes to illuminate complex host-parasite coevolutionary dynamics.

Sociality and disease: behavioral perspectives in ecological and evolutionary immunology

“…Host sociality can drive pathogen/parasite evolution. Janecka et al (2021), using guppies as a model, stress the importance of recognizing the role that host social behavior has on generating fine-scale changes in the spatial distribution of parasite genotypes, their influence on parasite non-random mating, gene flow, genetic drift, changes in population effective size, bottlenecks, genetic diversity, and, ultimately, parasite virulence and host/parasite coevolutionary history. Interestingly, Moore et al ( 2021) add yet another level of complexity to host/pathogen coevolution.…”

Predation shifts coevolution toward higher host contact rate and parasite virulence

“…Many animal taxa, invertebrates [22] and vertebrates [23] alike, group for defence against predators. For prey infected with parasites that rely on contact or proximity for transmission, grouping may strongly influence parasite transmission and, ultimately, evolution [24,25]. In such cases, increased predation effectively increases the cost of parasite avoidance.…”

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

“…Unfortunately, our understanding of how river architecture and hosts may interact to influence parasite genetic diversity and transmission in riverine systems is largely unknown (Blasco-Costa et al . 2012, 2013; Blasco-Costa & Poulin 2013; Janecka et al . 2021b).…”

“…Riverine parasites also cause significant morbidity and mortality to fish of conservation (Lymbery et al 2020) and commercial concern (Krkosek et al 2007). Unfortunately, our understanding of how river architecture and hosts may interact to influence parasite genetic diversity and transmission in riverine systems is largely unknown (Blasco-Costa et al 2012Janecka et al 2021b).…”