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A Double-Edged Sword: Parental care increases risk of offspring infection by a maternally-vectored parasite

Citation

Millena, Rebecca Jean; Rosenheim, Jay (2022), A Double-Edged Sword: Parental care increases risk of offspring infection by a maternally-vectored parasite, Dryad, Dataset, https://doi.org/10.5061/dryad.qnk98sfjg

Abstract

Parental care can protect offspring from predators but can also create opportunities for parents to vector parasites to their offspring. We hypothesized that the risk of infection by maternally-vectored parasites would increase with the frequency of mother-offspring contact. Ammophila spp. wasps (Hymenoptera: Sphecidae) build nests in which they rear single offspring. Ammophila species exhibit varied offspring provisioning behaviors: some species enter the nest once to provision a single, large caterpillar, whereas others enter the nest repeatedly to provision with many smaller caterpillars. We hypothesized that each nest visit increases the risk of offspring parasitism by Paraxenos lugubris (Strepsiptera: Xenidae), whose infectious stages ride on the mother wasp (phoresy) to reach the vulnerable Ammophila offspring. We quantified parasitism risk by external examination of museum-curated Ammophila specimens—the anterior portion of P. lugubris protrudes between the adult host’s abdominal sclerites and reflects infection during the larval stage. As predicted, Ammophila species that receive larger numbers of provisions incur greater risks of parasitism, with nest provisioning behavior explaining ca. 90% of the interspecific variation in mean parasitism. These findings demonstrate that parental care can augment, rather than reduce, risk of parasite transmission to offspring.

Methods

We gathered records of the provisioning behavior for Californian species of Ammophila from the literature. Using “Ammophila” and “provisioning” as terms, we conducted searches via the Web of Science, BIOSIS, and Google Scholar search engines. We supplemented the published literature with our own unpublished field observations. When multiple provisioning records existed for a species, we calculated an average across the studies to produce a single estimate for the mean prey provisioned.

These data were gathered via examination of all specimens of Ammophila housed in the Bohart Museum of Entomology, University of California, Davis. Parasitized Ammophila specimens stored in the Strepsiptera collections were also included in our dataset. Paraxenos lugubris develops as an endoparasite, but its anterior end protrudes visibly from the abdomen of its host as it completes its development, allowing parasitism to be recorded in museum-preserved specimens. We examined each specimen with a stereomicroscope and scored for the presence or absence of Paraxenos. Wasps were scored as parasitized when they had a female Paraxenos still present in their abdomen, or when they had a male Paraxenos either still present and enclosed in a pupal casing, or previously-emerged from the abdomen, leaving behind a still-visible pupal exoskeleton (winged males emerge from their host to seek out females for mating, whereas the wingless females never leave their hosts). We also recorded Ammophila wing length as an index of host size, and the collection date for each specimen. Our final data set included all 16 species for which established estimates of mean prey provisioned were available. We scored a total of 8957 specimens collected between 1902 and 2009. All data were recorded in Excel, and the spreadsheet plus its metadata are available here.

Parasitism data were analyzed with a generalized linear mixed model with binomial variance and a logistic link function, using the R package lme4. An additional analysis involving phylogenetic contrasts run with the R package ape is included as an R script. A third R script contains the code for each visualized linear analysis. View README.txt for details about necessary R package versions.

Usage Notes

In the document “ammophila_strep_project.csv”, null or 0 values should be left blank (with the exception of 0 values in columns "parasitism", "m_strep", and "f_strep"). One README file is available detailing the package versions used for each of the R scripts in this collection. Metadata/data description is available as a tab in the raw data Excel file.

Funding

University of California Leadership Excellence through Advanced Degrees (UC LEADS)