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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 statement

Social 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.

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Fig. 1
Fig. 2

adapted from Thomaz et al. 2016)—the inset color graph represents local population genetic identity in multivariate space. Asymmetric dispersal in response to unidirectional stream drift results greater genetic diversity downstream and in narrower parasite transmission bottlenecks farther upstream, increasing the strength of genetic drift upstream (see Fig. 3)

Fig. 3
Fig. 4

Data availability

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Code availability

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Acknowledgements

We thank the editors of this special topical collection and three anonymous reviewers for their insightful and constructive comments on this manuscript.

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Support for this review was provided by NSF (MJJ DEB: 2010826 and FR DGE: 1747452) and the University of Pittsburgh (JFS).

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Conceptualization: MJJ, JFS. Writing—original draft preparation: MJJ, FR, JFS. Writing—review and editing: MJJ, FR, JFS.

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Janecka, M.J., Rovenolt, F. & Stephenson, J.F. How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale?. Behav Ecol Sociobiol 75, 150 (2021). https://doi.org/10.1007/s00265-021-03089-y

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Keywords

  • Host social behavior
  • Host-parasite coevolution
  • Landscape population genetics
  • Spatial scale
  • Parasite non-selective evolution
  • Parasite transmission dynamics