Bottom–up regulates top–down: the effects of hybridization of grass endophytes on an aphid herbivore and its generalist predator

Abstract

The ecological consequences of hybridization of microbial symbionts are largely unknown. We tested the hypothesis that hybridization of microbial symbionts of plants can negatively affect performance of herbivores and their natural enemies. In addition, we studied the effects of hybridization of these symbionts on feeding preference of herbivores and their natural enemies. We used Arizona fescue as the host‐plant, Neotyphodium endophytes as symbionts, the bird cherry–oat aphid as the herbivore and the pink spotted ladybird beetle as the predator in controlled experiments. Neither endophyte infection (infected or not infected) nor hybrid status (hybrid and non‐hybrid infection) affected aphid reproduction, proportion of winged forms in the aphid populations, aphid host‐plant preference or body mass of the ladybirds. However, development of ladybird larvae was delayed when fed with aphids grown on hybrid (H+) endophyte infected grasses compared to larvae fed with aphids from non‐hybrid (NH+) infected grasses, non‐hybrid, endophyte‐removed grasses (NH−) and hybrid, endophyte‐removed (H−) grasses. Furthermore, adult beetles were more likely to choose all other types of grasses harboring aphids rather than H+ infected grasses. In addition, development of ladybirds was delayed when fed with aphids from naturally uninfected (E−) grasses compared to ladybirds that were fed with aphids from NH+ and NH− grasses. Our results suggest that hybridization of microbial symbionts may negatively affect generalist predators such as the pink spotted ladybird and protect herbivores like the bird cherry–oat aphids from predation even though the direct effects on herbivores are not evident.

Fungal endophytes of Festuca rubra increase in frequency following long-term exclusion of rabbits

“…By contrast, studies in native grass systems, although fewer in number, have reported higher herbivore abundances on endophyte-infected plants (Jani et al 2010;Faeth and Shochat 2010). However, the effects of endophytes on herbivore performance and communities are highly variable and dependent upon many factors, including soil moisture and nutrients (Saikkonen et al 2006(Saikkonen et al , 2010aSaona et al 2010), plant genotype (Yurkonis et al 2014), types and concentrations of endophyte produced alkaloids (Jani et al 2010), endophyte reproductive strategy (Tintjer and Rudgers 2006), endophyte hybridization (Saari et al 2014), and herbivore identity and diet breadth (Hartley and Gange 2009;Afkhami and Rudgers 2009). In our system, for example, F. rubra is a preferred food source for rabbits and grazing often results in decreased abundance of this grass (Crawley 1990).…”

Anti‐insect defenses of Achnatherum robustum (sleepygrass) provided by two Epichloë endophyte species

“…For example, insect species may have individual susceptibility to various alkaloidal compounds (Siegel et al, 1990;Crawford et al, 2010;Schardl et al, 2013). Further complicating the picture is that endophytic alkaloids could be sequestered by the insect herbivore and used as defense against their own natural enemies (Saari et al, 2014).…”

“…Correlative and experimental field studies showed that an endophyte from the Cloudcroft population may affect arthropods similar to other Epichloë spp. Infection and its associated alkaloids reduce abundances of arthropod predators or parasitoids, negatively affect generalist herbivores, and provide enemy‐free space for specialized herbivores that are capable of alkaloid detoxification and sequestering for their own defense (Jani et al., ; Faeth & Saari, ; Saari et al., ). Insect bioassays using the generalist herbivore Rhopalosiphum padi (L.) indicate that aphids did not survive on infected plants originating from the Cloudcroft population (Shymanovich et al., ).…”

“…Direct protection against insect herbivores may be due to insecticidal compounds such as loline alkaloids Nformylloline, N-acetylnorloline, and the ergot alkaloid ergovaline or due to insect-deterring alkaloidal compounds such as peramine (Rowan et al, 1986;Potter et al, 2008;Jensen et al, 2009;Popay et al, 2009). Specific fungal alkaloid compounds from all four classes may cause delayed development and reduced mass and fecundity, which may decrease insect fitness and therefore indirectly reduce insect population sizes and densities (Braman et al, 2002;H€ arri et al, 2008;Dmitriew & Rowe, 2011;Saari et al, 2014;V elez et al, 2014).…”

Does hybridization of endophytic symbionts in a native grass increase fitness in resource‐limited environments?

“…Rather there are other factors, such as interactions with herbivores and natural enemies (e.g., Saari et al. ) or relative fitness measures related to plant genotype that dictate the distribution of hybrid infected plants in nature.…”