Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects

The relationship between oviposition preference and growth, survival, and reproduction of offspring is the crux of the problem in the evolution of host associations between phytophagous insects and plants. Observed relationships between oviposition preference and performance of offspring range from good to poor. At least four hypotheses have been suggested to explain observed use of particular host plants that may not result in the fastest growth rates or greatest pupal masses: time, patch dynamics, parasite versus grazer lifestyles, and enemy-free space. Our current understanding of these relationships, however, is hampered by an almost complete lack of data on how preference and performance are related genetically. These data are needed to understand the origins of covariance between preference and performance and constraints on the evolution of host associations.     

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.     

Preference–performance relationship in the gall midge Rabdophaga rosaria: insights from a common‐garden experiment with nine willow clones

1. Oviposition preferences of herbivorous insects are predicted to match offspring performance on different host taxa or on conspecific host genotypes. In gall‐inducing insects, host‐plant properties such as growth rate and gall size, which are determined by plant genotype and growing conditions, may have a significant impact on offspring performance and, hence, should influence oviposition site selection. 2. The present study investigated host preference of the European rosette willow gall midge Rabdophaga rosaria (Loew) in relation to offspring success on seven clones of Salix myrsinifolia Salisb. and two naturally hybridised S. myrsinifolia × phylicifolia L. clones growing in a replicated design in an experimental field under two fertilisation regimes. For each clone, the average growth rate, number of shoot tips, and leaf and gall size were determined, and their effects on midge preference and larval survival were examined. 3. Main shoot height, number of shoot tips, and gall size were significantly affected by clone. The midges clearly preferred certain clones over the others, but preferences were not related to willow growth traits or to gall size. Survival probability was higher in large than in small galls, but females did not prefer large‐leaved clones that produced the biggest rosette galls. Midge oviposition was also uncorrelated with prior rates of leaf‐rust infection and with feeding preferences of voles and folivorous insects. 4. The weak preference–performance relationship of R. rosaria within S. myrsinifolia is probably explained by evolutionary constraints that prevent generalist insects from achieving an ability to discriminate among conspecific hosts of variable quality.     

Inconsistent use of host plants by the Alaskan swallowtail butterfly: adult preference experiments suggest labile oviposition strategy

Abstract 1. The Alaskan swallowtail butterfly (Papilio machaon aliaska) uses three unrelated plant species as hosts: Cnidium cnidiifolium (Apiaceae), Artemisia arctica (Asteraceae), and Petasites frigidus (Asteraceae). The research presented here investigated whether there are any consistent patterns in host choice by P. m. aliaska females. 2. The first two experiments were designed to test if P. m. aliaska host preference is constant or if it changes from day to day. If host preference is labile, the experiments were designed to also test whether a female’s diet breadth narrows or expands over time. 3. The third experiment tested the host preferences of female offspring from several wild-caught P. m. aliaska females. If P. m. aliaska individuals are specialised in their host use, then all of the offspring from a single female would likely prefer the same host-plant species. This experiment was also designed to test the Hopkins’ host selection principle; does the food plant on which a female is reared as a larva influence her future choices when she is searching for host plants for her own offspring? 4. The results from all of these experiments indicate that P. m. aliaska females vary greatly in their oviposition behaviour and in their preferences for the three host plants. Most populations appear to consist of generalists with labile oviposition behaviour. There is no evidence to support the Hopkins’ host selection principle. 5. It is suggested that the generalised selection of host plants by P. m. aliaska females may be a ‘bet-hedging’ strategy and that this strategy may maximise reproductive fitness in an unpredictable environment.     

Influence of larval experience on preference of a subterranean insect Delia antiqua on Allium hosts

Numerous studies have reported that larval experience can affect subsequent host plants selection and future oviposition decisions of many different species, but the investigation of pre‐imaginal experiences on host preference of adults has rarely been tested for soil‐dwelling insects. In this study, we present evidence that larval feeding experience can affect adult host preference in the onion maggot, Delia antiqua. By rearing D. antiqua on different host plants, we were able to examine the role of the natal host of different generations and the effect of larval density on host‐choice behaviour. We also performed bioassays by means of switched host treatment to evaluate the host‐selection principle. Choice bioassays among the three host species demonstrated that D. antiqua females preferred to oviposit on their natal host in each generation and host‐switching treatments. Additionally, increasing larval density could intensify this ovipositional preference on the natal host. The overall results showed that host preference of female D. antiqua is determined by larval experience and density. These findings also add support for the controversial Hopkins’ host‐selection principle.     

桔小实蝇和番石榴实蝇对6种寄主果实的产卵选择适应性

植食性昆虫对寄主植物的选择适应性是研究昆虫和植物协同进化关系的核心内容之一。评估寄主植物对植食性昆虫种群的适合度,需要综合分析昆虫对寄主的产卵选择性和寄主对昆虫的取食适合性。以桔小实蝇和番石榴实蝇为研究对象,分别测定了这两种实蝇对6种寄主果实:番石榴、香蕉、杨桃、木瓜、甜橙、番茄的产卵选择性以及幼虫取食后对其生长发育的影响。寄主产卵选择性实验分别采用完整寄主果实直接供试产卵和块状寄主果实气味引诱产卵两种处理方式;在生长发育适应性实验中,以幼虫和蛹的存活和生长发育等相关参数作为评价指标。实验结果表明,寄主的供试方式不同,两种实蝇的选择性均有明显差异;对寄主气味选择性强的寄主更适合于两种实蝇后代的生长发育。两种实蝇对6种寄主果实的产卵选择性和后代发育适合性两者相关性不显著,与许多文献报道单一地采用发育适合性(如发育历期、存活率或蛹重等)作为评价寄主选择性的结果不一致。两种实蝇之间对6种寄主果实的产卵选择和幼虫取食适合性既具相似性也具差异性,表明这两种实蝇在寄主生态位上既有重叠性又有分化性。     

Plant architecture affects periodical cicada oviposition behavior on native and non‐native hosts

Variation in plant quality provides a basis for oviposition site selection for a variety of insects. Of the plant traits that influence plant–insect interactions, plant architecture has received little attention despite its putative role in modulating oviposition behavior. In a common garden comprised of native and non‐native plant species, we assessed how host plant architecture and identity influenced the oviposition behavior of 17‐year periodical cicadas (Homoptera: Cicadidae: Magicicada). On each host, we quantified the availability of branches suitable for oviposition and compared those measures with the branches used by ovipositing cicadas. Using this approach, we determined how the structural attributes of plants (i.e. branch diameter, length and incline) affected oviposition site selection. We then related cicada oviposition preferences to offspring performance by quantifying egg hatching success. On each host species, cicadas selectively used broader and longer branches for oviposition, suggesting that branch architecture provides a basis for oviposition behavior irrespective of plant identity. Broader and longer branches were more abundant on native than on non‐native hosts in our study, contributing to greater oviposition loads among the native species. Egg hatching success was similar among native and non‐native hosts. However, it is possible that the use of native plants for oviposition could enhance offspring output because native hosts generally contained more viable eggs per egg nest and more egg nests per plant. While previous accounts of cicada oviposition preferences have focused on differences in oviposition loads among hosts, our evaluation of within‐host branch selection by ovipositing cicadas helps to clarify oviposition preferences at a higher resolution and demonstrates that plant architecture provides an important basis for oviposition behavior. Furthermore, because branch structure can differ substantially among host species, our results suggest that periodical cicadas may be sensitive to the changes in plant composition that often result from non‐native plant invasions.     

Oviposition site preference and developmental performance of a gall‐inducing leafhopper on galled and non‐galled host plants

Oviposition preferences of herbivorous insects affect offspring performance. Both positive and negative links between oviposition preference and offspring performance have been reported for many species. A gall‐inducing leafhopper, Cicadulina bipunctata Melichar (Hemiptera: Cicadellidae), feeds on various Poaceae plants and induces galls of enhanced nutritional value for their offspring. Although gall induction by C. bipunctata improves nymphal performance, the oviposition preference of females between galled and non‐galled host plants is still unclear. In this paper, the nymphal performance and oviposition and feeding‐site preference of C. bipunctata were investigated using galled wheat, Triticum aestivum L., and non‐galled barley, Hordeum vulgare L., as host plants. The survival rate of C. bipunctata on wheat was significantly higher than on barley. In the choice test, significantly more eggs were laid into barley, whereas the number of eggs deposited on both hosts was not significantly different in the no‐choice test. The number of settling individuals per leaf area was not significantly different between wheat and barley, suggesting no clear preference for oviposition between these plants. Experience as a nymph with a growing host did not affect oviposition preference as adult female. The inconsistent correspondence between offspring performance and oviposition preference of C. bipunctata may reflect the high mobility of nymphs and/or differences in leaf area between host plants. The results indicate that the previous finding that oviposition preference and offspring performance are not always positively correlated in herbivorous insects is applicable to gall‐inducing insects.     

The Relationship Between Habitat Selection and Preference for Adult and Larval Food Resources in the Polyphagous Butterfly <Emphasis Type="Italic">Vanessa cardui</Emphasis> (Lepidoptera: Nymphalidae)

Search strategies can have profound fitness-effects for plant-feeding insects. Here I focus on the potential conflict between searching for nectar plants and for larval food plants. I test if the butterfly Vanessa cardui, which can use some of its larval food plants as nectar sources, is able to rationalize this search problem by combining the two search tasks. Lab-experiments revealed a higher oviposition preference for Cirsium arvense over Urtica dioica and a corresponding difference in larval performance. Contrary to predictions, there was no effect of inflorescences on oviposition. However, experiments in large outdoor cages showed a higher occupancy and a higher level of oviposition in patches with access to nectar sources, even on U. dioica. Hence, while there was no preference for individual plants with flowers, the results suggests that V. cardui is simplifying its search task to primarily search for hosts in nectar-rich patches. This strategy allows females to increase oviposition rate, but it is likely that it comes at the expense of not always using optimal host plants in terms of offspring performance.     

EVOLUTIONARY GENETICS OF OVIPOSITION PREFERENCE IN SWALLOWTAIL BUTTERFLIES

Models of the evolution of host shifts and speciation in phytophagous insects are often built upon the assumption that host selection is under simple genetic control, perhaps even a single locus. The genetic basis for differences in host-plant preference by ovipositing insects was investigated using two closely related species of swallowtail butterfly, Papilio oregonius and P. zelicaon, which differ in the plant families on which females oviposit. Both species had been shown previously to vary within populations in host selection. A combination of analyses using reciprocal interspecific crosses and isofemale strains within populations indicated that oviposition preference in these species is determined significantly by one or more loci on the X chromosome, which female Lepidoptera inherit only paternally. Hence, preferences in hybrid females tended toward the paternal species. This is the first insect group for which partial control of oviposition preference has been localized onto a particular chromosome. In addition, one or more loci on another chromosome(s) appear to contribute to preference, as indicated by the partially intermediate preferences of some hybrid crosses. The overall differences in preference in the reciprocal interspecific hybrids were restricted to differences in the distribution of eggs laid among the local host plants of these two Papilio species; the reciprocal crosses did not differ in the small percentage of eggs laid on a novel potential host species. The variation in host selection found among the isofemale strains reinforces earlier results for these strains, indicating that there is genetic variation in host selection within these populations. Overall, the results indicate that the evolution of oviposition preference in these species involves genetic changes at two or more chromosomes with the X chromosome playing an important role in determining preference.     

A RECENT HOST RANGE EXPANSION IN JUNONIA COENIA HÜBNER (NYMPHALIDAE): OVIPOSITION PREFERENCE,SURVIVAL, GROWTH,AND CHEMICAL DEFENSE

This paper reports on an investigation of two populations of Junonia coenia, the buckeye butterfly, one that feeds on the species' typical host plant (Plantago lanceolata) and one that utilizes a novel host plant (Kickxia elatine). I examined these populations for local adaptive responses in terms of oviposition behavior, growth, and chemical defense, on both P. lanceolata and K. elatine. In addition, I examined the genetic architecture underlying these traits using a full-sib quantitative genetic analysis. I found that a significant majority of females prefer the host plant species found at their collection sites in oviposition tests, but that there is no evidence that they are locally adapted in growth performance, as measured by fifth-instar and pupal weights and development times. Neither are there correlations between oviposition preferences of females and the growth performance or levels of chemical defense of their offspring. The two populations studied do, however, show specialization in terms of the levels of chemical defense they sequester from their host plants. I argue that these results indicate that natural enemies are the normal barriers to host range expansion in this oligophagous herbivore because a breakdown in those barriers results in genetic changes that enhance resistance to predation. This is despite the fact that adaptive responses in physiology are unlikely to be limited by a lack of genetic variability; the genetic architecture among traits would be conducive to specialization in growth performance; and there are costs to chemical defense in this species. All these conditions would tend to argue that J. coenia harbors considerable potential for coevolutionary interactions with its chemically defended hosts, but this potential is not realized, probably because natural selection on diet breadth by natural enemies is much stronger than selection from host plants in this system.     

Optimal foraging shapes host preference of a polyphagous leafminer

Abstract.  1. Most research on host selection by arthropods is based on optimal oviposition theory. This theory, also called the oviposition preference–offspring performance hypothesis, predicts that a female will choose those hosts for oviposition on which larvae perform best. Recent studies suggested, however, that optimal foraging by adults, or the quality of the host for adult performance, might also influence host choice.
2. This study investigated whether host preference of the polyphagous leafminer Liriomyza trifolii is determined by optimal foraging and/or optimal oviposition.
3. Female realised fecundity correlated nearly perfectly with feeding and oviposition preference of L. trifolii . The relationships between host preference and the offspring performance measures were always weaker. Hosts optimal for adult nutrition were also optimal for offspring performance but not vice versa . Hence, it was concluded that optimal foraging shapes feeding and oviposition preference of L. trifolii as this is the best strategy in order to maximise female fitness.     

Superparasitism of larval hosts by the walnut fly, <Emphasis Type="Italic">Rhagoletis juglandis</Emphasis>, and its implications for female and offspring performance

The oviposition-preference–offspring-performance hypothesis predicts that female insects should prefer to deposit clutches on or in hosts that maximize offspring performance. An important assumption behind this prediction is that female fitness is tightly correlated with the fitness of any one offspring. In this study, we evaluate offspring performance in the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), in relation to a previously described oviposition preference for previously exploited host fruit. In particular, we examined how superparasitism of walnut hosts influences offspring survival and weight at pupation under field conditions. We found that superparasitism was common and that increases in larval densities within fruit were associated with reduced larval survival and weight at pupation. In a laboratory experiment, female size was correlated with lifetime fecundity. In this system, oviposition preference is therefore negatively, not positively, correlated with offspring performance. We argue that patterns of female preference in this system reflect direct benefits to females that are traded off against costs in terms of offspring fitness. Because female fitness is a product not only of offspring quality but also of the total number of offspring produced, female walnut flies may be optimizing their fitness by producing many less fecund offspring. Studies examining the preference-performance hypothesis should consider the reproductive conflicts between parents and offspring as potential factors that influence the congruence between parental preference and offspring performance.     

Discrimination within and between host species by a butterfly: implications for design of preference experiments

Experiments designed to reveal variation among individual parasites in preference for different host species may generate misleading results. Apparent variation in the order of preference among host species can be generated solely from variation in the strength of discriminations made within host species. We illustrate this with a study of oviposition preference in the butterfly Melitaea cinxia. All butterflies were tested on the same six individual plants, three Plantago lanceolata (P) and three Veronica spicata (V). Some insects repeatedly preferred all individual P over all individual V or vice versa. We designated these as "pure" species ranks. Other insects repeatedly produced "mixed" ranks, preferring some individual V over some P, and some individual P over some V. We show how a "mixed" rank butterfly could differ from a "pure" rank insect by discriminating either more within plant species and/or less between them. Therefore, discrimination within host species can mask or confound discrimination among species. We discuss implications for the design of preference experiments.     

No effect of larval experience on adult host preferences in Polygonia c‐album (Lepidoptera: Nymphalidae): on the persistence of Hopkins’ host selection principle

Abstract 1. The possible effect of juvenile imprinting or ‘chemical legacy’ on the subsequent oviposition – often called the ‘Hopkins’ host selection principle’– has been a controversial but recurrent theme in the literature on host‐plant preference. While it appears possible in principle, experimental support for the hypothesis is equivocal. The present study points out that it is also important to consider its theoretical implications, and asks under what circumstances, if any, it should be favoured by natural selection. 2. Following this reasoning, it is predicted that host preference in the polyphagous butterfly Polygonia c‐album L. (Lepidoptera, Nymphalidae) should not be influenced by larval environment. This was tested by rearing larvae on three natural host plants: the high‐ranked Urtica dioica and the medium‐ranked Salix cinerea and Ribes uva‐crispa, and exposing the naive females to oviposition choices involving the same set of plants. 3. It was found that larval host plant had no effect on oviposition decisions of the adult female. Hence, the Hopkins’ host selection principle does not seem to be applicable in this species. 4. Based on recent insights on how accuracy of environmental versus genetic information should affect the control of developmental switches, the conditions that could favour the use of juvenile cues in oviposition decisions are discussed. Although the Hopkins’ host selection hypothesis cannot be completely ruled out, we argue that the circumstances required for it to be adaptive are so specific that it should not be invoked as a general hypothesis for host selection in plant‐feeding insects.     

Oviposition site selection by herbivorous beetles: a comparison of two thistle feeders, Cassida rubiginosa and Henosepilachna niponica

In insects that feed on plants in both adult and larval stages, it is often difficult to distinguish oviposition preference from adult feeding preference, because oviposition can occur at or in proximity to feeding sites. In the present study, characteristics of oviposition site selection of two beetle species, Cassida rubiginosa Müller (Coleoptera: Chrysomelidae) and Henosepilachna niponica (Lewis) (Coleoptera: Coccinellidae), were investigated in the field and laboratory, with particular attention to relationships with adult feeding sites. In the field, distances between adult feeding scars and egg masses differed for C . rubiginosa and H . niponica , with the former being very small and the latter averaging 24.6 cm. The same tendencies for the distances between adult feeding scars and egg masses of the two beetle species were confirmed in cages in which only female beetles were released. Cassida rubiginosa restricted egg laying to host plants in the field and to leaves in laboratory assays. On the other hand, H . niponica placed 8% of egg masses on plants adjacent to host plants in the field and often placed eggs on artificial substrates rather than leaf discs in laboratory assays. These results suggest that oviposition and female feeding sites are virtually inseparable in the case of C . rubiginosa , while H . niponica females do not necessarily keep to host plant leaves as oviposition substrates and they tend to oviposit at some distance from their feeding sites. Results are discussed in relation to proximate and ultimate causes of host selection behavior.     

Counteracting selective regimes and host preference evolution in ecotypes of two species of walking-sticks

The evolution of ecological specialization has been a central topic in ecology because specialized adaptations to divergent environments can result in reproductive isolation and facilitate speciation. However, the order in which different aspects of habitat adaptation and habitat preference evolve is unclear. Timema walking-stick insects feed and mate on the host plants on which they rest. Previous studies of T. cristinae ecotypes have documented divergent, host-specific selection from visual predators and the evolution of divergent host and mate preferences between populations using different host-plant species (Ceanothus or Adenostoma). Here we present new data that show that T. podura, a nonsister species of T. cristinae, has also formed ecotypes on these host genera and that in both species these ecotypes exhibit adaptive divergence in color-pattern and host preference. Color-pattern morphs exhibit survival trade-offs on different hosts due to differential predation. In contrast, fecundity trade-offs on different hosts do not occur in either species. Thus, host preference in both species has evolved before divergent physiological adaptation but in concert with morphological adaptations. Our results shed light onto which traits are involved in the initial stages of ecological specialization and ecologically based reproductive isolation.     

Host preference of the bean weevil Zabrotes subfasciatus

It is largely known that the range of an insect diet is mostly determined by oviposition behavior, mainly in species with endophytic larvae such as Zabrotes subfasciatus. However, the proximate factors determining host choice and the subsequent steps leading to the expansion or reduction of the host number and occasional host shifts are largely unknown. We analyzed various factors determining host preference of Z. subfasciatus through the evaluation of: (i) oviposition preference of a wild population of Z. subfasciatus on the usual host (bean) and unusual hosts (lentil, chickpea and soy), and the performance of the offspring; (ii) artificial selection for increasing preference for hosts initially less frequently chosen; (iii) comparison of oviposition behavior between two different populations (reared for ∼30 generations in beans or chickpeas, respectively); (iv) oviposition timing on usual and unusual hosts; and (v) identification of preference hierarchies. We found that when using unusual hosts, there is no correlation between performance and preference and that the preference hierarchy changes only slightly when the population passes through several generations on the less frequently accepted host. We also found a positive response to artificial selection for increasing oviposition on the less preferred host; however, when the host-choice experiment involved two varieties of the usual host, the response was faster than when the choice involved usual and unusual hosts. Finally, beetles reared on an unusual host (chickpea) for 26 generations showed similar good fitness on both usual and unusual hosts, indicating that the use of a new host does not necessarily result in the loss of performance on the original host. Nevertheless, this population showed lower fitness on the usual host than that of the original population, suggesting an underlying partial trade-off phenomenon which may contribute to a broadening of diet of this insect species.     

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.     

Relationship between oviposition preference and offspring performance in Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Abstract We investigated the oviposition preference and larval performance of Helicoverpa armigera under laboratory conditions to determine if the oviposition preference of individual females on maize, cowpea and cotton correlates with offspring performance on the leaves of the same host plants. The host-plant preference hierarchy of females did not correlate with their offspring performance. Female moths chose host plants that contributed less to their offspring fitness. Plant effects accounted for the largest amount of variation in offspring performance, while the effects of female (family) was low. The offspring of most females (80%, n  = 10) were broadly similar, but 20% (two out of 10), showed marked difference in their offspring performance across the host-plant species. Similarly, there was no relation between larval feeding preference and performance. However, like most laboratory experiments, our experi-mental design does not allow the evaluation of ecological factors (for example, natural enemies, host abundance, etc.) that can play an important role in larval performance in the field. Overall, the results highlight the importance of carrying out preference performance analysis on the individual or family level, rather than pooling individuals to obtain average population data.