Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids

Abstract

Insects use endogenous mechanisms and infection with protective symbionts to thwart attacks from natural enemies. Defenses that target specific enemies, however, potentially mediate competition between rivals and thereby impact community composition. Following its introduction to North America to control pea aphids (Acyrthosiphon pisum), the parasitoid Aphidius ervi competitively displaced other parasitoids, except for the native Praon pequodorum. The pea aphid exhibits tremendous clonal variation in resistance to A. ervi, primarily through infection with the heritable bacterial symbiont Hamiltonella defensa, although some symbiont-free aphid genotypes encode endogenous resistance. Interestingly, H. defensa strains and aphid genotypes that protect against A. ervi, provide no protection against the closely related, P. pequodorum. Given the specificity of aphid defenses, we hypothesized that aphid resistance traits may contribute to the continued persistence of P. pequodorum. We conducted multiparasitism assays to determine whether aphid resistance traits mediate internal competition between these two solitary parasitoid species, but found this was not the case; P. pequodorum was the successful internal competitor across lines varying in susceptibility to A. ervi. Next, to determine whether resistance traits influence competitive interactions resulting in the stable persistence of P. pequodorum, we established replicated cages varying in the proportion of resistant aphids and recorded successful parasitism for each wasp species over time. As expected, A. ervi outcompeted P. pequodorum in cages containing only susceptible aphids. However, P. pequodorum not only persisted, but was the superior competitor in populations containing any proportion (20–100%) of resistant aphids (20–100%). Smaller scale, better replicated competition cage studies corroborated this finding, and no-competition and behavioral assays provide insight into the processes mediating competition. Genetic variation, including that acquired via infection with protective symbionts, may provide a supply of hosts susceptible only to particular enemies, mediating competition with effects on community richness and stability.

Does getting defensive get you anywhere?—Seasonal balancing selection, temperature, and parasitoids shape real‐world, protective endosymbiont dynamics in the pea aphid

“…This pattern fits a previously published trend in which high Hamiltonella prevalence in pea aphid populations predicted low mummification rates, and vice versa (Smith et al, 2015). So while the selective agents behind defensive symbiont prevalence may be, sometimes, obscure, the spread of such symbionts may have numerous consequences for eco‐evolutionary feedbacks and surrounding ecological communities (Clay et al, 2005; Ives et al, 2020; Jaenike & Brekke, 2011; Kraft et al, 2017; McLean et al, 2017; Rothacher et al, 2016; Sanders et al, 2016; terHost & Zee, 2016).…”

Culture-Facilitated Comparative Genomics of the Facultative Symbiont Hamiltonella defensa

“…2017 ), while also differentially affecting parasitoid competitive interactions in the same host ( Oliver et al. 2012 ; McLean and Godfray 2015 ; Kraft et al. 2017 ).…”

Positive association between the diversity of symbionts and parasitoids of aphids in field populations

“…The presence or absence of symbionts can drive the abundance of parasitoids and the composition of parasitoid communities both in the laboratory (Sanders et al 2016, Kraft et al 2017, Käch et al 2018) and in the field (Hrček et al 2016, Rothacher et al 2016). Protective symbionts impose selection on parasitoids, forcing them to evolve to overcome resistance (Dion et al 2011, Rouchet and Vorburger 2014, Dennis et al 2017).…”