A double-edged sword: parental care increases risk of offspring infection by a maternally vectored parasite

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 a single offspring. Ammophila species exhibit varied offspring provisioning behaviours: 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 behaviour explaining ca 90% of the interspecific variation in mean parasitism. These findings demonstrate that parental care can augment, rather than reduce, the risk of parasite transmission to offspring.

Nesting behavior of the solitary ground-nesting wasp Ammophila boharti Menke, 1963 (Hymenoptera: Sphecidae)

“…Solitary ground-nesting wasps in the genus Ammophila W. Kirby, 1798 have long attracted the attention of researchers interested in the evolution of subsocial behavior, as the genus is speciose (Pulawski 2023), with 62 species known from North America (Menke 2020), and behaviorally diverse, including members with different degrees of extended parental care (Evans & West-Eberhard 1970). Ammophila species also exhibit remarkably intricate nest construction behavior and diverse strategies to defend their nests against a suite of nest parasites (e.g., Rosenheim 1987, Field & Brace 2004, Millena & Rosenheim 2022). Field et al (2020) have recently used a molecular phylogeny to show that an early hypothesis that wasp behavior evolved through a regular series of unidirectional transitions towards greater parental care (the ‘stepping stone’ or ‘social ladder’ model for the evolution of subsociality (see Linksvayer & Johnson 2019)) is not supported; instead, behavioral transitions appear to be frequent in both directions, both towards and away from more extended parental care.…”