Host plant resistance promotes a secondary pest population

Straub, Cory S.; Faselt, Jamie A; Keyser, Erich S.; Traugott, Michael

doi:10.1002/ecs2.3073

Cited by 11 publications

(9 citation statements)

References 49 publications

(61 reference statements)

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“…However, it is possible that non‐target insect pests are indirectly influenced. This was shown recently for pea aphid ( Acyrthosiphon pisum ), which was at least partly promoted by release from potato leafhopper ( Empoasca fabae ) competition due to insecticide application (Straub et al, 2020), and this indirect effect is also applicable to Bt‐crops (Zeilinger et al, 2016). The latter authors have reported a competitive release and outbreak of non‐target pests in transgenic Bt‐cotton.…”

Section: Insect Pest Resistance Breeding Approachesmentioning

confidence: 76%

Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north‐western Europe

Miedaner

Juroszek²

2021

Plant Pathology

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Maize productivity is threatened by global climate change. Climate change scenarios suggest that north‐western (NW) Europe will get warmer and drier during the main crop‐growing period. In general, more northerly regions will benefit, whereas more southerly regions will suffer suboptimal rain‐fed farming conditions. In these latter regions in particular, the resulting probable lower realized on‐farm maize grain and biomass yields must be safeguarded. Breeding for resistance against already existing and emerging diseases and insect pests is one component to achieve yield stability across years. Durable multiple‐disease resistance will become especially crucial. Herein, we focus on disease resistance breeding approaches in maize, especially related to northern corn leaf blight and Fusarium ear rots, although virus and bacterial diseases will become more important as well. Continuous adjustments of disease resistance breeding strategies will be required. Insect pest resistance breeding must be improved considerably, as in a warmer world insects will thrive, probably causing detrimental direct (feeding, sucking, etc.) and indirect (vectors of pathogens, feeding wounds creating gateways for many pathogens, passive transport of inoculum across maize plants) effects. Four case studies on insects that are already prevalent in NW Europe or may be expected in the near future are covered in this review. Maize cultivars need to combine both durable multiple‐disease and multiple‐insect resistance, although the implementation of many different effective resistance resources in breeding programmes will be challenging, particularly if trade‐offs among breeding goals appear.

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Section: Insect Pest Resistance Breeding Approachesmentioning

confidence: 76%

Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north‐western Europe

Miedaner

Juroszek²

2021

Plant Pathology

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“…ervi parasitoids, and ladybug predators (Coccinellidae) – two insect groups from a diverse community of alfalfa‐associated arthropods that were emphasized due to their large impacts on pea aphids. We also made counts of potato leafhoppers, potential pea aphid competitors (e.g., Straub et al, 2020), that trigger “hopperburn” damage on alfalfa plants.…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2021

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Facultative, heritable endosymbionts are found at intermediate prevalence within most insect species, playing frequent roles in their hosts’ defence against environmental pressures. Focusing on Hamiltonella defensa, a common bacterial endosymbiont of aphids, we tested the hypothesis that such pressures impose seasonal balancing selection, shaping a widespread infection polymorphism. In our studied pea aphid (Acyrthosiphon pisum) population, Hamiltonella frequencies ranged from 23.2% to 68.1% across a six‐month longitudinal survey. Rapid spikes and declines were often consistent across fields, and we estimated that selection coefficients for Hamiltonella‐infected aphids changed sign within this field season. Prior laboratory research suggested antiparasitoid defence as the major Hamiltonella benefit, and costs under parasitoid absence. While a prior field study suggested these forces can sometimes act as counter‐weights in a regime of seasonal balancing selection, our present survey showed no significant relationship between parasitoid wasps and Hamiltonella prevalence. Field cage experiments provided some explanation: parasitoids drove modest ~10% boosts to Hamiltonella frequencies that would be hard to detect under less controlled conditions. They also showed that Hamiltonella was not always costly under parasitoid exclusion, contradicting another prediction. Instead, our longitudinal survey – and two overwintering studies – showed temperature to be the strongest predictor of Hamiltonella prevalence. Matching some prior lab discoveries, this suggested that thermally sensitive costs and benefits, unrelated to parasitism, can shape Hamiltonella dynamics. These results add to a growing body of evidence for rapid, seasonal adaptation in multivoltine organisms, suggesting that such adaptation can be mediated through the diverse impacts of heritable bacterial endosymbionts.

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“…In addition to counts of pea aphids (winged and unwinged), we also censused A. ervi parasitoids , ladybug predators (Coccinellidae), and potato leafhoppers ( Empoasca fabae ). The former two insects are large sources of pea aphid mortality that may be thwarted by facultative symbionts [ 98 , 99 ], while the latter is a potential competitor of the pea aphid, e.g., [ 100 ]. Insect counts, climate data, and mortality assay data (below) can be found in Table S2 .…”

Section: Methodsmentioning

confidence: 99%

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

Carpenter

Peng

Smith

et al. 2021

Insects

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Insects harbor a variety of maternally inherited bacterial symbionts. As such, variation in symbiont presence/absence, in the combinations of harbored symbionts, and in the genotypes of harbored symbiont species provide heritable genetic variation of potential use in the insects’ adaptive repertoires. Understanding the natural importance of symbionts is challenging but studying their dynamics over time can help to elucidate the potential for such symbiont-driven insect adaptation. Toward this end, we studied the seasonal dynamics of six maternally transferred bacterial symbiont species in the multivoltine pea aphid (Acyrthosiphon pisum). Our sampling focused on six alfalfa fields in southeastern Pennsylvania, and spanned 14 timepoints within the 2012 growing season, in addition to two overwintering periods. To test and generate hypotheses on the natural relevance of these non-essential symbionts, we examined whether symbiont dynamics correlated with any of ten measured environmental variables from the 2012 growing season, including some of known importance in the lab. We found that five symbionts changed prevalence across one or both overwintering periods, and that the same five species underwent such frequency shifts across the 2012 growing season. Intriguingly, the frequencies of these dynamic symbionts showed robust correlations with a subset of our measured environmental variables. Several of these trends supported the natural relevance of lab-discovered symbiont roles, including anti-pathogen defense. For a seventh symbiont—Hamiltonella defensa—studied previously across the same study periods, we tested whether a reported correlation between prevalence and temperature stemmed not from thermally varying host-level fitness effects, but from selection on co-infecting symbionts or on aphid-encoded alleles associated with this bacterium. In general, such “hitchhiking” effects were not evident during times with strongly correlated Hamiltonella and temperature shifts. However, we did identify at least one time period in which Hamiltonella spread was likely driven by selection on a co-infecting symbiont—Rickettsiella viridis. Recognizing the broader potential for such hitchhiking, we explored selection on co-infecting symbionts as a possible driver behind the dynamics of the remaining six species. Out of twelve examined instances of symbiont dynamics unfolding across 2-week periods or overwintering spans, we found eight in which the focal symbiont underwent parallel frequency shifts under single infection and one or more co-infection contexts. This supported the idea that phenotypic variation created by the presence/absence of individual symbionts is a direct target for selection, and that symbiont effects can be robust under co-habitation with other symbionts. Contrastingly, in two cases, we found that selection may target phenotypes emerging from symbiont co-infections, with specific species combinations driving overall trends for the focal dynamic symbionts, without correlated change under single infection. Finally, in three cases—including the one described above for Hamiltonella—our data suggested that incidental co-infection with a (dis)favored symbiont could lead to large frequency shifts for “passenger” symbionts, conferring no apparent cost or benefit. Such hitchhiking has rarely been studied in heritable symbiont systems. We propose that it is more common than appreciated, given the widespread nature of maternally inherited bacteria, and the frequency of multi-species symbiotic communities across insects.

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Host plant resistance promotes a secondary pest population

Cited by 11 publications

References 49 publications

Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north‐western Europe

Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north‐western Europe

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

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

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