Research Article: Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids

Date Published: July 10, 2017

Publisher: Public Library of Science

Author(s): Laura J. Kraft, James Kopco, Jason P. Harmon, Kerry M. Oliver, Nicolas Desneux.


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.

Partial Text

Diverse eukaryotic taxa show substantial variation in susceptibility to attack by specific natural enemies [1–5]. Most insect species, for example, are attacked by parasitoids, which typically kill their host before completing development, resulting in strong selection for hosts with resistance traits [6, 7]. Resistance to attack, however, can be costly, often leading to variation among individuals within a species [8–10]. Host resistance to parasitoids can be endogenous or mediated by infection with microbial symbionts, and each type of resistance may be specialized to particular natural enemies [11–17]. Variation and specialization in resistance to particular enemies may affect competitive interactions among parasitoid species [2, 18] and ultimately influence the species richness and evenness of the parasitoid community attacking the host.

In North American pea aphid field populations, A. ervi is the dominant parasitoid, having competitively displaced numerous native and introduced parasitoids other than P. pequodorum, which remains at low levels in most sampled fields [38]. Using population cages, we show that both symbiont-based and endogenous aphid resistance traits can impact competition between these two rival parasitoids allowing for the persistence of P. pequodorum. In cages containing only aphids susceptible to attack by A. ervi, this wasp outcompetes and displaces P. pequodorum. However, in cages containing any proportion of aphids infected with the protective symbiont H. defensa (from 20 to 100%), or those with 100% endogenous resistance, P. pequodorum maintained viable populations for multiple generations and even displaces A. ervi in most instances (Figs 1 and 2). The finding that symbiont-resistance favors P. pequodorum was recapitulated in smaller, better replicated arenas (Fig 4). Thus, symbiont and host resistance traits likely provide a reservoir of susceptible hosts available only to P. pequodorum allowing this wasp to remain in natural populations when other species have been displaced. Consistent with this hypothesis, we found that P. pequodorum does equally well on all aphid lines in our no-competition assays, while A. ervi performance varies depending on the proportion of aphids with symbiont-based resistance (Fig 3). Such target-specific traits may impact community structure by differentially affecting species at higher trophic levels contributing to community richness and evenness.

Here we show that aphid resistance traits from both endogenous and symbiont-based sources can influence competition between rival parasitoids, even when found at low percentages (20%) within populations. This result likely contributes to the persistence of P. pequodorum in field populations after the establishment of A. ervi, which displaced other parasitoids [38]. Thus, bacterial symbionts can play roles in influencing the composition of natural enemies attacking their hosts. Moreover, defensive symbionts and other resistance traits are may be more likely to target co-evolved enemies (but see [55]), and thus be less likely to harm native parasitoids that move onto the introduced host.




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