Role of parasite transmission in promoting inbreeding: I. Infection intensities drive individual parasite selfing rates

Detwiler, Jillian T.; Caballero, Isabel; Criscione, Charles D.

doi:10.1111/mec.14211

Cited by 16 publications

(39 citation statements)

References 62 publications

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“…Mediterranean geckos were collected in College Station, Texas, USA. Details of sampling locations and collection protocols were described previously (Detwiler & Criscione, , ; Detwiler et al., ). Briefly, cestodes were still alive upon dissection.…”

Section: Methodsmentioning

confidence: 99%

“…() call for additional studies from understudied animal clades. For instance, despite species estimates upwards of 130,000 (Strona & Fattorini, ), the predominantly hermaphroditic parasitic flatworms (Neodermata: trematodes, cestodes and monogenes) have received little attention regarding the estimation of either primary selfing rates or ID (Benesh, Weinreich, Kalbe, & Milinski, ; Criscione, ; Detwiler, Caballero, & Criscione, ).…”

Section: Introductionmentioning

confidence: 99%

“…A recent study estimated individual maternal tapeworm selfing rates via progeny‐array data of metacestode genotypes and thus after the passage through an intermediate host (Detwiler et al., ). They found that individual selfing rates were highly correlated (inverse power relationship) to the number of tapeworms within a host, that is the infection intensity (Detwiler et al., ). Using the distribution of parasites among hosts and assuming random reproductive success, Detwiler et al.…”

Section: Introductionmentioning

confidence: 99%

“…Using the distribution of parasites among hosts and assuming random reproductive success, Detwiler et al. () estimated the population selfing rate to be 30.6% (average across five subpopulations using GLMM estimates; figure 2 in Detwiler et al. ()).…”

Section: Introductionmentioning

confidence: 99%

“…() estimated the population selfing rate to be 30.6% (average across five subpopulations using GLMM estimates; figure 2 in Detwiler et al. ()). Hence, O. javaensis has a mixed‐mating system as estimated at the metacestode stage.…”

Section: Introductionmentioning

confidence: 99%

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Little to no inbreeding depression in a tapeworm with mixed mating

Caballero

Criscione

2019

J of Evolutionary Biology

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Meta‐studies on hermaphrodites have found a negative relationship between primary selfing rates and levels of inbreeding depression (ID) and, thus, generally support purging in inbred systems. However, in plants, high among‐taxa variance in ID results in no difference in the mean ID between outcrossing and mixed‐mating taxa. Selective interference likely explains high ID among mixed‐mating taxa, whereas low levels of ID among mixed‐mating taxa are not as stressed. Among animal hermaphrodites, primarily molluscs, there are little data on mixed‐mating systems. To fill a taxonomic and mating system gap, we tested for ID in a mixed‐mating tapeworm, Oochoristica javaensis. We provide a direct estimate of ID across infection of an intermediate host by comparing selfing rates at two life history stages. We found little to no evidence for ID, and the level of ID falls in line with what is reported for highly selfing species even though O. javaensis has mixed mating. We discuss this result within the context of kin mating in O. javaensis. Our results emphasize that primary selfing rates alone may be insufficient to classify the inbreeding history in all species when testing for a relationship to ID. Mixed‐mating taxa, and possibly some outcrossing taxa, may exhibit low levels of ID if biparental inbreeding is also driving purging. We advocate that ID studies report estimates of inbreeding history (e.g. FIS or identity disequilibrium) from nature‐derived adult samples to provide context rather than relying on primary selfing rates alone.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Little to no inbreeding depression in a tapeworm with mixed mating

Caballero

Criscione

2019

J of Evolutionary Biology

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

Janecka

Rovenolt

Stephenson

2021

Behav Ecol Sociobiol

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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.

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