Innate preference hierarchies coupled with adult experience,rather than larval imprinting or transgenerational acclimation,determine host plant use in Pieris rapae

The evolution of host range drives diversification in phytophagous insects, and understanding the female oviposition choices is pivotal for understanding host specialization. One controversial mechanism for female host choice is Hopkins’ host selection principle, where females are predicted to increase their preference for the host species they were feeding upon as larvae. A recent hypothesis posits that such larval imprinting is especially adaptive in combination with anticipatory transgenerational acclimation, so that females both allocate and adapt their offspring to their future host. We study the butterfly Pieris rapae, for which previous evidence suggests that females prefer to oviposit on host individuals of similar nitrogen content as the plant they were feeding upon as larvae, and where the offspring show higher performance on the mother's host type. We test the hypothesis that larval experience and anticipatory transgenerational effects influence female host plant acceptance (no‐choice) and preference (choice) of two host plant species (Barbarea vulgaris and Berteroa incana) of varying nitrogen content. We then test the offspring performance on these hosts. We found no evidence of larval imprinting affecting female decision‐making during oviposition, but that an adult female experience of egg laying in no‐choice trials on the less‐preferred host Be. incana slightly increased the P. rapae propensity to oviposit on Be. incana in subsequent choice trials. We found no transgenerational effects on female host acceptance or preference, but negative transgenerational effects on larval performance, because the offspring of P. rapae females that had developed on Be. incana as larvae grew slower on both hosts, and especially on Be. incana. Our results suggest that among host species, preferences are guided by hard‐wired preference hierarchies linked to species‐specific host traits and less affected by larval experience or transgenerational effects, which may be more important for females evaluating different host individuals of the same species.     

Divergence in behaviour between the European corn borer,Ostrinia nubilalis,and its sibling species Ostrinia scapulalis: adaptation to human harvesting?

Divergent adaptation to host plant species may be the major mechanism driving speciation and adaptive radiations in phytophagous insects. Host plants can differ intrinsically in a number of attributes, but the role of natural enemies in host plant specialization is often underappreciated. Here, we report behavioural divergence between the European corn borer (ECB, Ostrinia nubilalis) and its sibling species Ostrinia scapulalis, in relation to a major enemy: humans. Harvesting maize imposes selective mortality on Ostrinia larvae: those located above the cut-off line of the stalk face almost certain death. We show that ECB larvae diapause closer to the ground than those of O. scapulalis, which is sympatric but feeds mainly on weeds. The difference in diapause height results from genetically determined differences in geotactic behaviour. ECB larvae descend towards the ground specifically at harvest time, increasing their chances of surviving harvesting by about 50 per cent over O. scapulalis larvae. Natural enemies appear as a major driver of host-plant specialization in this example, stressing the need to consider ‘tri-trophic’ ecological niches to understand insect diversification. Our results also strongly suggest that geotaxis evolved as a singular instance of behavioural resistance in a major agricultural pest.     

Neighbourhood of host plants influences oviposition decisions of a stem-boring weevil

The spatial arrangement of suitable host plants in the field may significantly constrain insects to find optimal hosts. Plant neighbours around a focal host plant can either lead to lower (associational resistance) or higher (associational susceptibility) herbivore loads. We tested whether the spatial arrangement of hosts of different suitability for the larval development of the shoot-base boring weevil Apion onopordi affects oviposition decisions in the field. Host plants in our study were healthy creeping thistles (Cirsium arvense; suboptimal hosts) and thistles infected by a rust pathogen (Puccinia punctiformis; optimal hosts). For analysis, we used nearest neighbour methods that disentangle the spatial distribution of organisms that are dependent on the position of other species (e.g. phytophagous insects and their host plants). Although theory predicts that the small-scale spatial infestation pattern can have major consequences for the population dynamics in insect–plant systems, field studies quantifying spatial pattern of phytophagous insects are rare.

The spatial arrangement of host plants clearly influenced oviposition pattern in A. onopordi. In contrast to previous studies, we demonstrated that not the rust infection itself determined if a plant was infested by weevils, but rather the density of rusted shoots within a certain neighbourhood. We found strong indications for associational susceptibility of healthy thistle shoots to weevil oviposition when growing in the neighbourhood of rusted thistles. Weevil-infested plants were spatially aggregated, indicating that A. onopordi is limited in its dispersal ability within patches. Other stem-boring insects on creeping thistle were affected in their oviposition decisions by other factors than A. onopordi. Thus, it may be difficult to find general rules for oviposition choice in phytophagous insects.

Our study showed that the spatial arrangement of host plants in the field critically determines oviposition choice and should thus be included as constraint in theories of optimal host selection.     

The role of nectar sources for oviposition decisions of the common blue butterfly Polyommatus icarus

Neural limitations on information processing have been shown to play an important role for host plant specialization in herbivorous insects. The necessity of fast and accurate decisions favors the adoption of a few high-contrast signals, which selects against the use of multiple resources. Many species face a similar problem when searching for adult food sources and the simultaneous need to fulfill both search tasks can lead to a potential conflict. Some insects use the same host plant species for both adult and larval nutrition, which makes it possible to decrease the number of search images and thus potentially increase efficiency of the choices. The aim of this study was to investigate if there is a connection between choice of nectar sources and choice of oviposition host plant. In a laboratory experiment, females of Polyommatus icarus preferred to oviposit on Lotus corniculatus plants with flowers over those without flowers. Observations of behavioral sequences also revealed that oviposition often followed immediately after nectaring. The results suggest that nectar availability could play an important role in oviposition decisions of P. icarus and can provide one explanation to why some phytophagous insects not always choose the host plant that gives the best offspring performance.     

Conserved oviposition preferences in alpine leaf beetle populations despite host shifts and isolation

Abstract.  1. Choosing the plant on which to lay their eggs is the last act of care that most female herbivorous insects bestow upon their offspring. These decisions play a pivotal role in insect–plant interactions, placing host preference under strong selection and contributing to the diversity of phytophagous insects as one of the first traits to adapt to new hosts.
2. This study presents a test of whether extreme isolation and exposure to different host plants can produce intra-specific divergence in oviposition preference in alpine insects. Geographic variation should impose selection to fine-tune host plant ranking and specificity to the plants normally encountered, to avoid wasting time during the very limited reproductive season experienced at high altitudes.
3. Beetles from five populations of Oreina elongata differing in host availability were offered three natural hosts: Cirsium spinosissimum , Adenostyles alliariae , and Adenostyles glabra . A novel application of a continuation ratio model (logistic regression) was made to sequential no-choice experiments, combined with quasi-likelihood analysis of multiple-choice experiments.
4. The results show little geographic variation in host plant choice: all populations strongly preferred Cirsium in multiple-choice trials, and in no-choice experiments laid around 47% of their remaining eggs during each stage, almost regardless of the host present.
5. Enemy-free space seems to explain the preference for Cirsium , but isolation and exposure to different plants has clearly not caused local adaptation in host plant ranking or specificity. Reasons for this conservatism despite divergence in other characteristics are discussed.     

Divergent host plant preference causes assortative mating between sympatric host races of the ladybird beetle,Henosepilachna diekei

Divergent host preference (i.e. host fidelity) plays a significant role in the speciation process in phytophagous insects. However, how and to what extent this divergence reduces gene flow between populations has rarely been measured. Here, we estimated the intensity of assortative mating caused solely by host fidelity in two host races of the phytophagous ladybird beetle Henosepilachna diekei, specialized on Mikania micrantha (Asteraceae) and Leucas lavandulifolia (Lamiaceae) in West Java, Indonesia. These host races mated randomly in the absence of host plants under laboratory conditions, but demonstrated nearly complete assortative mating in field cages with the two host plants, by spending almost all of their time on their respective host plants. The frequency of assortative mating in the field cages was not affected drastically by host plant patch structure. These results suggest that fidelity to the different host plants yields directly almost complete reproductive isolation between the host races by limiting the habitat on the respective host plant. In addition, the high host fidelity also ensures female oviposition on the original host plant. As larvae cannot survive on non‐host plants, a positive association between female oviposition preference and larval performance on the host plant on which the beetles are specialized will further facilitate the evolution of host fidelity. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 606–614.     

Adaptation to different host plant ages facilitates insect divergence without a host shift

Host shifts and subsequent adaption to novel host plants are important drivers of speciation among phytophagous insects. However, there is considerably less evidence for host plant-mediated speciation in the absence of a host shift. Here, we investigated divergence of two sympatric sister elm leaf beetles, Pyrrhalta maculicollis and P. aenescens, which feed on different age classes of the elm Ulmus pumila L. (seedling versus adult trees). Using a field survey coupled with preference and performance trials, we show that these beetle species are highly divergent in both feeding and oviposition preference and specialize on either seedling or adult stages of their host plant. An experiment using artificial leaf discs painted with leaf surface wax extracts showed that host plant chemistry is a critical element that shapes preference. Specialization appears to be driven by adaptive divergence as there was also evidence of divergent selection; beetles had significantly higher survival and fecundity when reared on their natal host plant age class. Together, the results identify the first probable example of divergence induced by host plant age, thus extending how phytophagous insects might diversify in the absence of host shifts.     

Host-plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa

Abstract.  1. During range expansions of phytophagous insects, secondary or novel hosts may allow colonisation of areas without primary hosts. Because plant species often differ in their relative attractiveness and suitability for insects, insect preference for, and performance on, these hosts can determine recruitment potential in the current and future expansion areas.
2. This study explores the relative roles of female preference and larval performance in an important pine defoliator, Thaumetopoea pityocampa (Denis & Schiffermüller) (Lepidoptera, Notodontidae), which colonises three Pinus species at its current range margin in the Italian Alps: P. nigra (primary host), P. sylvestris (secondary host), and P. mugo (novel host).
3. Host use patterns in multiple insect populations were studied through choice and no-choice oviposition experiments in cages, field surveys of mixed stands, and laboratory and field monitoring of larval growth and mortality. It was predicted that a specific life-history trait – time limitation of short-lived females to lay a single batch of eggs – would act as a component of female performance, and lead to similar rates of host acceptance in no-choice settings.
4. In the choice experiment, P. nigra was accepted the most frequently while P. sylvestris was accepted the least frequently, confirming nest density patterns in the field. Contrary to prediction, females remained discriminating in no-choice settings in spite of time limitation. In contrast, relative growth rate (RGR) and mortality of larvae did not differ significantly among the three hosts, highlighting a discrepancy between female preference and larval performance.
5. Recruitment potential of T. pityocampa in future expansion into stands of P. sylvestris and P. mugo is evaluated by combining host quality, conservatism in oviposition behaviour, habitat suitability, and the opportunity for local adaptation.     

Integrating optimal foraging and optimal oviposition theory in plant–insect research

The current approach for studying host selection by phytophagous insects is mainly based on optimal oviposition theory, i.e. the preference–performance hypothesis. Almost no attention has been given to optimal foraging theory. However, recent papers and additional evidence given in this work illustrate that also optimal foraging may shape host preference patterns of phytophagous insects. Therefore and because optimal foraging and optimal oviposition may oppose conflicting needs to phytophagous insects, we plea for an integration of optimal foraging and optimal oviposition in plant–insect research. We argue how this may improve our understanding of plant–insect interactions.     

Geographic host use variability and host range evolutionary dynamics in the phytophagous insect <Emphasis Type="Italic">Apagomerella versicolor</Emphasis> (Cerambycidae)

The high diversity of phytophagous insects has been explained by the tendency of the group towards specialization; however, generalism may be advantageous in some environments. The cerambycid Apagomerella versicolor exhibits intraspecific geographical variation in host use. In northern Argentina it is highly specialized on the herb Pluchea sagittalis (Asteraceae), while in central and southern areas it uses seven Asteraceae species. To study host species geographical variation from ecological and evolutionary perspectives, we investigated field host availability and use across a wide latitudinal range, and performed laboratory studies on insect oviposition preference and larval performance and mitochondrial DNA (mtDNA) variation in a phylogeographical framework. Geographic variation in host use was unrelated to host availability but was highly associated with laboratory oviposition preference, larval performance, and mtDNA variation. Genetic studies revealed three geographic races of A. versicolor with gene flow restriction and recent geographic expansion. Trophic generalism and oligophagy within A. versicolor seem to have evolved as adaptations to seasonal and spatial unavailability of the preferred host P. sagittalis in cooler areas of the species’ geographic range. No single genotype is successful in all environments; specialization may be advantageous in environments with uniform temporal and spatial host availability, while being a trophic generalist may provide an adaptive advantage in host-constrained environments.     

Cascading host-associated genetic differentiation in parasitoids of phytophagous insects

The extraordinary diversity of phytophagous insects may be attributable to their narrow specialization as parasites of plants, with selective tradeoffs associated with alternate host plants driving genetic divergence of host-associated forms via ecological speciation. Most phytophagous insects in turn are attacked by parasitoid insects, which are similarly specialized and may also undergo host-associated differentiation (HAD). A particularly interesting possibility is that HAD by phytophagous insects might lead to HAD in parasitoids, as parasitoids evolve divergent lineages on the new host plant-specific lineages of their phytophagous hosts. We call this process 'cascading host-associated differentiation' (cascading HAD). We tested for cascading HAD in parasitoids of two phytophagous insects, each of which consists of genetically distinct host-associated lineages on the same pair of goldenrods (Solidago). Each parasitoid exhibited significant host-associated genetic divergence, and the distribution and patterns of divergence are consistent with divergence in sympatry. Although evidence for cascading HAD is currently limited, our results suggest that it could play an important role in the diversification of parasitoids attacking phytophagous insects. The existence of cryptic host-associated lineages also suggests that the diversity of parasitoids may be vastly underestimated.     

Geographic variation in oviposition choice of a leaf beetle: the relationship between host plant ranking, specificity, and motivation

The degree of adaptation of herbivorous insects to their local flora is an important component of the evolutionary processes that lead to host plant specialization in insects. In this study we investigated geographic variations in the oviposition preference of the leaf beetle Oreina elongata Suffrian (Coleoptera: Chrysomelidae: Chrysolini) in relation to differences in host plant specialization, in the field. We focused on the mechanisms of host choice and asked whether potential differences among populations are due to variations in host plant ranking and/or host plant specificity. We performed a combination of simultaneous choice and sequential no‐choice experiments with two of the major host plants of the beetle [Cirsium spinosissimum (L.) and Adenostyles alliariae (Gouan) (Asteraceae)]. The results suggested that spatial variation in host plant specialization has resulted in differences between populations in some aspects of the oviposition choice of O. elongata, while other aspects seem unaffected. We found no variation in host plant ranking among populations, as estimated in simultaneous choice tests. In contrast, the sequential no‐choice test indicated that host plant specificity was lower in a population that never encountered the highest ranked plant in the field. This finding agreed with our expectations, and we discuss our results in relation to the commonly used hierarchical threshold model. The results suggested that the mechanism for the differences in specificity is the variation among populations in the general motivation to oviposit, rather than quantitative differences in relative preference for the two hosts. We stress that it is essential to establish which of the two mechanisms is most important, as it will affect the probability of evolutionary change in host plant ranking.     

Factors Influencing Host Plant Choice and Larval Performance in Bactericera cockerelli

Among the many topics of interest to ecologists studying associations between phytophagous insects and their host plants are the influence of natal host plant on future oviposition decisions and the mechanisms of generalist versus specialist host selection behavior. In this study, we examined the oviposition preferences, behavior and larval development of the tomato/potato psyllid, Bactericera cockerelli. By rearing psyllids with two distinct geographically-linked haplotypes on different host plants, we were able to examine the role of natal host plant and potential local adaptation on host plant usage. Choice bioassays among three host species demonstrated that psyllids from California had clear preferences that were influenced by natal plant. We further found that patterns in choice bioassays corresponded to observed feeding and movement responses. No-choice bioassays demonstrated that there is little to no association between development and host-plant choice for oviposition, while also indicating that host choice varies between haplotypes. These findings support the concept that mothers do not always choose oviposition sites optimally and also add support for the controversial Hopkins'' host selection principle.     

Butterfly oviposition preference is not related to larval performance on a polyploid herb

The preference–performance hypothesis predicts that female insects maximize their fitness by utilizing host plants which are associated with high larval performance. Still, studies with several insect species have failed to find a positive correlation between oviposition preference and larval performance. In the present study, we experimentally investigated the relationship between oviposition preferences and larval performance in the butterfly Anthocharis cardamines. Preferences were assessed using both cage experiments and field data on the proportion of host plant individuals utilized in natural populations. Larval performance was experimentally investigated using larvae descending from 419 oviposition events by 21 females on plants from 51 populations of two ploidy types of the perennial herb Cardamine pratensis. Neither ploidy type nor population identity influenced egg survival or larval development, but increased plant inflorescence size resulted in a larger final larval size. There was no correlation between female oviposition preference and egg survival or larval development under controlled conditions. Moreover, variation in larval performance among populations under controlled conditions was not correlated with the proportion of host plants utilized in the field. Lastly, first instar larvae added to plants rejected for oviposition by butterfly females during the preference experiment performed equally well as larvae growing on plants chosen for oviposition. The lack of a correlation between larval performance and oviposition preference for A. cardamines under both experimental and natural settings suggests that female host choice does not maximize the fitness of the individual offspring.     

Physical and chemical cues affect oviposition by Neoleucinodes elegantalis

Recognition and acceptance of a suitable host plant by phytophagous insects requires the integration of visual, physical and chemical cues. The present study investigates the host cues that a specialist insect integrates to optimize oviposition decisions and whether these cues are weighted in a specific way. The study also determines whether the tomato fruit borer Neoleucinodes elegantalis (Guenée) (Lepidoptera: Crambidae), an important pest on Solanaceae in Brazil, shows a preference for oviposition sites that differ in physical and/or chemical cues. When styrofoam balls are provided as artificial fruits, N. elegantalis deposit significantly more eggs on rough artificial fruits than on smooth ones. Hexane fruit extracts applied to the artificial fruits stimulate female oviposition strongly. Physical and chemical cues also affect the oviposition of females when offered together. Furthermore, certain parts of the artificial fruits are prefered, irrespective of the presence of chemical cues. Both physical and chemical cues affect oviposition decisions; hence, the fruit borer relies on cues of different sensory modalities.     

Experimental evidence of host race formation in Mitoura butterflies (Lepidoptera: Lycaenidae)

A population of herbivorous insects that shifts to a novel host can experience selection pressures that result in adaptation to the new resource. Host race formation, considered an early stage of the speciation process, may result. The current study investigates host shifts and variation in traits potentially involved in the evolution of reproductive isolation among populations of the juniper hairstreak butterfly, Mitoura gryneus. Mitoura are closely associated with their host trees (Cupressaceae) and exhibit host plant fidelity: in addition to larval development and oviposition, host trees support male leks and mating. Female oviposition preference for the natal host, and differential fitness of larvae when reared on natal versus alternate hosts, are indications that specialization and local adaptation to the natal host plant are occurring. Populations with single host plant associations (Juniperus ashei, J. pinchotii and J. virginiana) as well as populations with multiple hosts (both J. ashei and J. pinchotii) were examined. Concordance between female preference and larval performance was found for J. ashei‐associated populations. Population‐level variation in the patterns of female preference and larval performance, both within and among host associations, may reflect differences in the timing and direction of colonization of hosts. For a single nominal species that otherwise exhibits no morphological or phenological differences, the experimental assessment of specialization and host fidelity in M. gryneus provides strong support for the hypothesis of ongoing host race formation in these butterflies.     

When History Repeats Itself: Exploring the Genetic Architecture of Host-Plant Adaptation in Two Closely Related Lepidopteran Species

The genus Ostrinia includes two allopatric maize pests across Eurasia, namely the European corn borer (ECB, O. nubilalis) and the Asian corn borer (ACB, O. furnacalis). A third species, the Adzuki bean borer (ABB, O. scapulalis), occurs in sympatry with both the ECB and the ACB. The ABB mostly feeds on native dicots, which probably correspond to the ancestral host plant type for the genus Ostrinia. This situation offers the opportunity to characterize the two presumably independent adaptations or preadaptations to maize that occurred in the ECB and ACB. In the present study, we aimed at deciphering the genetic architecture of these two adaptations to maize, a monocot host plant recently introduced into Eurasia. To this end, we performed a genome scan analysis based on 684 AFLP markers in 12 populations of ECB, ACB and ABB. We detected 2 outlier AFLP loci when comparing French populations of the ECB and ABB, and 9 outliers when comparing Chinese populations of the ACB and ABB. These outliers were different in both countries, and we found no evidence of linkage disequilibrium between any two of them. These results suggest that adaptation or preadaptation to maize relies on a different genetic architecture in the ECB and ACB. However, this conclusion must be considered in light of the constraints inherent to genome scan approaches and of the intricate evolution of adaptation and reproductive isolation in the Ostrinia spp. complex.     

植食性昆虫的学习行为

学习是指因经历不同而导致的行为变化。在植食性昆虫中,学习主要包含习惯性反应、厌恶性学习、联系性学习、敏感性反应和嗜好性诱导等类型。昆虫在幼虫和成虫期都具有学习能力,但幼虫期食料和取食经历不会对成虫行为产生直接影响。昆虫学习行为的表现受其本身食性、寄主刺激物的类别及寄主植物时空分布动态等因子的影响。学习能力有助于植食性昆虫应对复杂多变的植物环境,提高对寄主植物的利用效率,有利于其生存繁衍。对害虫学习行为的了解可为栖境调控、行为调控等害虫治理方法提供重要     

Jack of one trade,master of none: host choice by Drosophila magnaquinaria

Summary Host selection by phytophagous insects is generally thought to be based on chemical or nutritional characteristics of the host. This is especially true for monophagous insects. However, many other factors may influence host choice. The present study examines host selection by Drosophila magnaquinaria, whose sole host is the yellow skunk cabbage, Lysichitum americanum. Utilization of skunk cabbage was tested relative to a set of alternative hosts. In the pre-alighting stage of host selection, skunk cabbage was found to be less attractive than tomato, cucumber, and commercial mushrooms. In pairwise oviposition tests, there were no differences among hosts. There were no differences in larval survivorship among skunk cabbage, tomato, cucumber, or Ramaria, and larvae developed into pupae earlier on tomato than on skunk cabbage. These results indicate that this monophagy is not based on characteristics of the host. We suggest that habitat selection is the more important factor in determining the association between D. magnaquinaria and skunk cabbage.     

Head shape variation in cerambycid saproxylic beetles as a function of host plant selection

Saproxylic insects depend on deadwood for larval development, and a certain degree of specialization may be involved in their choice of host plants and/or wood in a particular stage of degradation. The plant species chosen for oviposition in turn act as an environmental pressure on the head morphology of larvae and it is expected that head shape plasticity varies directly with the number of woody plant species used for larval development in each insect species. We analyzed head shape variation in saproxylic beetles with respect to host plant species, maximum time of larval emergence and season of the year when insects colonized branches. Generalist species in the use of host plants showed significant variation in head shape and size. Time of emergence and season did not appear to affect head shape, although season was a determinant factor of abundance and possibly head size variation.