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Modified, agricultural landscapes are susceptible to damage by insect pests. Biological control of pests is typically successful once a control agent has established, but this depends on the agent&rsquo, s capacity to co-evolve with the host. Theoretical studies have shown that different levels of genetic variation between the host and the control agent will lead to rapid evolution of resistance in the host. Although this has been reported in one instance, the underlying genetics have not been studied. To address this, we measured the genetic variation in New Zealand populations of the pasture pest, Argentine stem weevil (Listronotus bonariensis), which is controlled with declining effectiveness by a parasitoid wasp, Microctonus hyperodae. We constructed a draft reference genome of the weevil, collected samples from a geographical survey of 10 sites around New Zealand, and genotyped them using a modified genotyping-by-sequencing approach. New Zealand populations of Argentine stem weevil have high levels of heterozygosity and low population structure, consistent with a large effective population size and frequent gene flow. This implies that Argentine stem weevils were able to evolve more rapidly than their biocontrol agent, which reproduces asexually. These findings show that monitoring genetic diversity in biocontrol agents and their targets is critical for long-term success of biological control.

A growing awareness of human dependence on the natural capital of ecosystem services has highlighted the importance of such services to the sustainable management of both natural and production ecosystems. Biological control is an ecosystem service in which a pest, pathogen, or weed is effectively controlled through an ecological interaction (trophic or competitive) with its natural enemies, henceforth referred to as biological control agents (1). The control of an alien invasive species through the deliberate introduction of a specialist control agent from its geographic region of origin serves as one of the clearest examples of the value of biological control as an ecosystem service. A classic case is the successful control of the cassava mealybug ( Phenacoccus manihoti ) across the Central Belt of Africa following the introduction of a parasitoid wasp ( Anagyrus lopezi ) from South America (2). One surprising observation from the historical record of biological control is that although pests and weeds frequently become resistant to chemical pesticides (3), there has been no documented evidence of host resistance to an introduced parasitoid wasp (4). In PNAS, Tomasetto et al. (5) present the first clear example of the evolution of host resistance to an introduced parasitoid wasp from a study of the outcome of biological control of an invasive pasture weevil in New Zealand. The Argentine stem weevil ( Listronotus bonariensis ) was discovered in New Zealand in 1927 and became increasingly more damaging to grasslands with the intensification of livestock production in the 1980s. The deliberate introduction and establishment of an asexual population of a specialist parasitoid ( Microctonus hyperodae ) from South America in 1991 resulted in high levels of parasitism of adult weevils and successful suppression of the abundance of this invasive weevil. However, using a dataset on parasitism of overwintering Argentine stem weevils for the period from 1994 to 2015 … [↵][1]1Email: nmills{at}berkeley.edu. [1]: #xref-corresp-1-1

Sustainable and integrated pest management often involves insect parasitoids. However, the effectiveness of parasitoids biocontrol has often failed, frequently for obscure reasons. A parasitoid’s success is partly due to its behavioral response to pest density, i.e. its consumer functional response. For many years in New Zealand, a braconid parasitoid, Microctonus hyperodae successfully suppressed a severe ryegrass weevil pest, Listronotus bonariensis. However, there is now evidence that this has severely declined, but that the extent of decline can depend on the pasture species. Here, we tested whether the current functional responses of M. hyperodae to L. bonarensis in two of the most common New Zealand pasture grasses (Lolium multiflorum and L. perenne) reflect observed differences in field parasitism and whether this functional response has changed over time. Our analysis involved data both from 1993 and 2018. We found a type I functional response in L. multiflorum in both years, but the slope of the relationship declined over time. There was no evidence for any type of functional response in L. perenne. This lack of response in the L. perenne coincided with consistently found lower parasitism rates on this host plant than in L. multiflorum; both in the field and laboratory. Here, we found that apparently declining searching efficiency was correlated with the decline in parasitism. This observation supports the hypothesis that parasitism decline could be the result of evolution of resistance based on enhanced evasive behaviour by L. bonariensis.

Earlier study at a national scale has shown that insect pests in agriculture can develop resistance to natural enemies following ongoing expansion and simplification of agricultural systems. Here, we used 25 years of field-sampling data segmented into three distinct ecoregions in New Zealand to show that parasitism rate of a key pasture pest (Listronotus bonariensis, Argentine stem weevil) by the introduced parasitoid Microctonus hyperodae has significantly declined. However, this decline has not happened simultaneously in all three ecoregions but with a one year time-lag. The variation in parasitism rate trends might be attributed to subsets of the weevil populations that became resistant to their biocontrol agent once having been exposed to seven years selection pressure (ca. 14 generations) since the parasitoid releases. This result supports the hypothesis that adaptation leading to resistance might have similarly occurred in different parts of the country indicating that the genetic variation needed for the acquisition of resistance was equally present everywhere.

The Panel on Plant Health performed a pest categorisation of Listronotus bonariensis (Coleoptera: Curculionidae), the Argentine stem weevil, for the EU. L. bonariensis is a well-de fi ned species, recognised as a serious pest of pasture grasses, especially Lolium spp. and Poa annua , in New Zealand, and a rare pest of cereals in Argentina, Brazil and New Zealand. Larvae feed within the tillers and stems of grasses; adults can cut emerging cotyledons although they usually graze on leaves. Larval damage is most serious. Larval feeding causes a reduction in pasture quality that impacts on the production of grazing animals. L. bonariensis is not known to occur in the EU and is listed in Annex IIAI of Council Directive 2000/29/EC. L. bonariensis established in New Zealand via imported grass seeds and has been intercepted on grass seeds entering the EU. Considering the climatic similarities of the regions where the pest occurs and the very great extent to which hosts are grown across the EU, L. bonariensis has the potential to establish within the EU with two or three generations possible per year. Impacts could occur in grassland pastures and perhaps occasionally in cereals. In New Zealand, endophytic fungi occurring on potential hosts deter L. bonariensis from ovipositing on leaves and are toxic to larvae. Whether endophytic fungi on grasses in Europe could provide some resistance to L. bonariensis is uncertain. Phytosanitary measures are available to reduce the likelihood of introduction of this weevil . L. bonariensis fi ts all of the criteria assessed by EFSA to satisfy the de fi nition of a Union quarantine pest . L. bonariensis does not meet the criterion of occurring in the EU territory for it to be regarded as a Union regulated non-quarantine pest.

Some insects are infected with maternally inherited bacterial endosymbionts that protect them against pathogens or parasitoids. The weevil Sitona obsoletus (=Sitona lepidus) is invasive in New Zealand, and suspected to contain such defensive symbionts, because it is particularly resistant to a Moroccan strain of the parasitoid Microctonus aethiopoides (which successfully attacks many other weevil species), and shows geographic variation in susceptibility to an Irish strain of the same parasitoid. Using 454 pyrosequencing, we investigated the bacterial community associated with S. obsoletus, two other exotic weevils (Sitona discoideus and Listronotus bonariensis) and two endemic New Zealand weevils (Irenimus aequalis and Steriphus variabilis). We found that S. obsoletus was infected by one strain of Wolbachia and two strains of Rickettsia, none of which were found in any other weevil species examined. Using diagnostic PCR, we found that S. obsoletus in the Northland region, where parasitism is highly variable, were primarily infected with Wolbachia and Rickettsia strain 2, indicating that these two symbionts should be investigated for potential defensive properties. In comparison, S. discoideus lacked any apparent maternally inherited bacterial endosymbionts. In the other weevil species, we found a different strain of Wolbachia and two different strains of Spiroplasma. Two weevil species (St. variabilis and L. bonariensis) were infected with distinct strains of Nardonella, the ancestral endosymbiont of weevils, whereas three weevil species (S. obsoletus, S. discoideus, and I. aequalis) lacked evidence for Nardonella infection. However, I. aequalis was consistently infected with a novel Enterobacteriaceae strain, suggesting that a symbiont replacement may have taken place, similar to that described for other weevil clades.

The Argentine stem weevil, Listronotus bonariensis, is an important pest in pastures, especially ryegrass (Lolium sp.), compromising grassland persistence and productivity. Both, adult and specially larvae cause severe damage, action that generate the death of the tiller and reducing forage production. Chemical control has limited effectiveness in adult’s insect and negative effects on the environmental and toxicity to pollinators when applied close to the flowering period is observed. Therefore, the main currently strategy is based on the use of cultivars of Lolium endophyte fungus-infected with Neothypodium genus. However, over a decade that there are no reports on the presence of this weevil in southern Chile. Hence, the aim of this research was report the actual incidence of L. bonariensis in ryegrass pastures. The results of two years of prospecting showed that this weevil is currently causing damage to the ryegrass pastures indicating that the effectiveness of species infected with the fungus must be evaluated.

Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.

Field parasitism rates of the Argentine stem weevil Listronotus bonariensis (Kuschel; Coleoptera: Curculionidae) by Microctonus hyperodae Loan (Hymenoptera: Braconidae) are known to vary according to different host Lolium species that also differ in ploidy. To further investigate this, a laboratory study was conducted to examine parasitism rates on tetraploid Italian Lolium multiflorum, diploid Lolium perenne and diploid hybrid L. perenne ×L. multiflorum; none of which were infected by Epichloë endophyte. At the same time, the opportunity was taken to compare the results of this study with observations made during extensive laboratory-based research and parasitoid-rearing in the 1990s using the same host plant species. This made it possible to determine whether there has been any change in weevil susceptibility to the parasitoid over a 20 year period when in the presence of the tetraploid Italian, diploid perennial and hybrid host grasses that were commonly in use in the 1990’s. The incidence of parasitism in cages, in the presence of these three grasses mirrored what has recently been observed in the field. When caged, weevil parasitism rates in the presence of a tetraploid Italian ryegrass host were significantly higher (75%) than rates that occurred in the presence of either the diploid perennial (46%) or the diploid hybrid (52%) grass, which were not significantly different from each other. This is very different to laboratory parasitism rates in the 1990s when in the presence of both of the latter grasses high rates of parasitism (c. 75%) were recorded. These high rates are typical of those still found in weevils in the presence of both field and caged tetraploid Italian grasses. In contrast, the abrupt decline in weevil parasitism rates points to the possibility of evolved resistance by the weevil to the parasitoid in the diploid and hybrid grasses, but not so in the tetraploid. The orientation of plants in the laboratory cages had no significant effect on parasitism rates under any treatment conditions suggesting that plant architecture may not be contributing to the underlying mechanism resulting in different rates of parasitism. The evolutionary implications of what appears to be plant-mediated resistance of L. bonariensis to parasitism by M. hyperodae are discussed.

Listronotus bonariensis (Argentine stem weevil) is a stem-boring weevil that has become a major pasture pest in New Zealand, and cool climate turf grass in Australia. This species is also frequently found in native tussock grassland in New Zealand. Laboratory and field trials were established to determine the risk posed to both seedlings and established plants of three native grass species compared to what happens with a common host of this species, hybrid ryegrass (L. perenne X L. multiflorum). Adult weevil feeding damage scores were higher on Poa colensoi and Festuca novae-zelandiae than Chionochloa rigida. Oviposition was lower on P. colensoi than hybrid ryegrass, and no eggs were laid on F. novae-zelandiae. In field trials using the same four species established as spaced plants L. bonariensis laid more eggs per tiller in ryegrass in a low altitude pasture site than in ryegrass in a higher altitude site. No eggs were found on the three native grass species at the tussock sites, and only low numbers were found on other grasses at the low altitude pasture site. Despite this, numbers of adult weevils were extracted from the plants in the field trials. These may have comprised survivors of the original weevils added to the plants, together with new generation weevils that had emerged during the experiment. Irrespective, higher numbers were recovered from the tussock site plants than from those from the pasture site. It was concluded that L. bonariensis is likely to have little overall impact, but a greater impact on native grass seedling survival than on established plants.

A laboratory study was conducted to: (1) advance earlier work to determine the susceptibility of Listronotus bonariensis (Argentine stem weevil) to its parasitoid biological control agent, Microctonus hyperodae, in the presence of diploid ryegrasses such as Lolium multiflorum or Lolium perenne; and (2) determine whether or not plant orientation (i.e. horizontal vs. vertical) had any effect on parasitism rates. No significant differences in parasitism rates were found in the Listronotus bonariensis populations in the two grasses. However, combining and analysing these data with those from an earlier experiment conducted in the same way showed that parasitism rates were significantly lower in diploid Lolium multiflorum cultivars than in tetraploid Lolium multiflorum. This is the first clear evidence of a ploidy effect on parasitism rates in the presence of Lolium multiflorum. Tetraploid Lolium multiflorum has fewer, more robust and larger tillers than the diploid Lolium spp. so higher parasitism rates may be related to the lack of hiding places for an evasive genetically-driven behaviourally-based resistance by Listronotus bonariensis.