Choosy mothers pick challenging plants: maternal preference and larval performance of a specialist herbivore are not linked

1. Maternal preference is a dynamic process and interactions between preference and performance are fundamental for understanding evolutionary ecology and host association in insect–plant interactions. In the present study, the hypothesis of preference–performance was tested by offering solanaceous specialist Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) larvae and adult females four plant congeners that ranged in suitability. 2. Larval feeding, development, oviposition, plant glycoalkaloids, and headspace volatiles in the four plant species were analysed to examine the extent of variation, which might explain performance–preference differences. 3. It was found that larval performance was mismatched with adult oviposition preferences. Adults laid more eggs on Solanum immite Dunal plants, which were poor hosts for larval development, feeding, and survival, compared to the other three Solanum species. 4. Chemical plant defenses, in general, did not correlate with performance or preference, but some plant volatiles may have played a role in resolving female choice. Glycoalkaloids such as solanine and chaconine were detected in similar amounts in preferred and non‐preferred hosts, but there was significantly more limonene in the headspace of S. immite than in S. tuberosum L. 5. The present findings suggest that we must consider the risk‐spreading hypothesis in cases where preference and performance are not positively correlated, particularly in specialist herbivores that can feed on a diversity of congener plants and may attempt to expand their exploits to other solanaceae species.     

Leaf wilting alters a plant species ranking by the grasshopper Melanoplus differentialis

Abstract. 1. Field observations of the feeding behaviour of the polyphagous grasshopper Melanoplus differentialis suggest that plant quality can override plant species as a determinant of choice. When offered binary choices in laboratory tests between leaves of two host plant species, Helianthus annuus and Ambrosia trifida , in all combinations of wilted and turgid, grasshoppers prefer A. trifida in all test conditions, except when it is turgid and H.annuus is wilted. In this case, the preference switches to H.annuus
2. Preliminary evidence suggests that chemical factors are responsible for the alteration in preference.     

双斑长跗萤叶甲的嗜食性

双斑长跗萤叶甲Monolepta hieroglyphica(Motschulsky)是一种多食性害虫。目前该虫害已成为新疆北部大部分棉区一种新的主要害虫。通过非选择性实验研究双斑长跗萤叶甲在新疆北疆的取食范围,结果表明:在25科54属58种植物中,该虫喜食植物有25种,较喜食植物有21种,完全不取食的有12种。     

The evolution of diet breadth: Monophagy and polyphagy in swallowtail butterflies

Much of the world's biodiversity has resulted from specialization of insect populations onto different plant species, partially through evolution of preference in ovipositing females. Here I report an experimental analysis of how an oviposition preference hierarchy has evolved during the evolutionary diversification of an insect group to produce taxa ranging from monophagous to polyphagous. Tests on the Papilio machaon group of swallowtail butterflies show that the preference hierarchy for plant species is evolutionarily dynamic within this species complex, yet constrained among most populations within species, creating a geographic mosaic of populations differing to various degrees in patterns of host preference. The results indicate that different diet breadths can evolve within a group of closely-related species through a combination of conservatism in preference hierarchy among some populations, occasional but rare rearrangements in preference among others, correlations in preference for some plant species, and availability of similarly ranked hosts.     

Population and individual polyphagy in the grasshopperTaeniopoda eques during natural foraging

Dietary patterns of free-foraging individuals of the polyphagous grasshopperTaeniopoda eques Burmeister (Romaleidae) were studied at three desert grassland sites in southern Arizona. At the population level this species was highly polyphagous at all sites, but showed evidence of selectivity in terms of frequency of feeding relative to frequency of contacts with resources. Most feeding bouts were very short, suggesting that most plants were relatively unpalatable. Both diet diversity and the mean length of feeding bouts varied among the study sites, primarily because highly preferred resources and plant tissues were not encountered with equal frequency at all sites. Individual insects were highly polyphagous. Dietary overlap calculations showed that insects at a given site generally consumed diets less similar than the resources they contacted. This result does not support the idea that all insects preferred the same subset of resources. Most differences in diet among individuals were probably due to environmental heterogeneity, but factors such as sequence of encounter, compensatory feeding on complementary resources, and intrinsic differences in preference may also have contributed to variation in diets.     

多食性斑潜蝇对寄主植物的选择

综述了有关斑潜蝇对寄主植物选择的研究进展。斑潜蝇对寄主植物的选择表现为对植物组织的选择、对植物不同部位叶片的选择、对同种植物不同品种的选择、对不同寄主植物的选择四个方面。斑潜蝇对寄主植物的选择主要受叶表面的物理性质、植物叶的化学物质成分、成长经历等因素的影响。阐述了多食性斑潜蝇寄主植物范围扩大的原因。     

Individual variation in two host plants of the ladybird beetle,Epilachna pustulosa (Coleoptera: Coccinellidae)

Individual variation in two species of host plants (thistle,Cirsium kamtschaticum, and blue cohosh,Caulophyllum robustum) of the herbivorous ladybird beetleEpilachna pustulosa was examined under laboratory conditions for their acceptability to adult beetles as a food resource, for adult preference and for larval performance. When clones of these plants were subjected to non-choice tests using posthibernating female beetles, there was found to be significant intraspecific variation among clones in terms of their acceptability, but interspecific variation was not detected. Significant intraspecific as well as interspecific variation were frequently detected in the two host plants when clones of these plants were subjected to choice tests using posthibernating female beetles; the magnitude of interspecific plant variation for beetle preference is not necessarily larger than that of intraspecific plant variation. Individual variation across plant species with respect to beetle larval performance was also significant. A positive correlation between adult preference and larval performance is suggested across the two taxonomically remote host plant species, thistle and blue cohosh, although this needs further investigation.     

Oviposition,larval preference,and larval performance in two polyphagous species: does the larva know best?

It is expected that females preferentially oviposit on plant hosts that allow for optimal larval performance. However, this expectation contradicts empirical evidence where adults do not always choose the best host for their descendants. Recent evidence suggests that females’ host selection depends on the number of potential hosts. Females from oligophagous species seem to be able to choose an appropriate host in terms of larval performance, whereas in polyphagous species, adult oviposition preference is not related with larval performance. This suggests that larvae in polyphagous species could be taking a more active role in host selection than their mothers. Here, we evaluated the oviposition preference and the larval preference and performance of two polyphagous species of economic importance, Copitarsia decolora (Guenée) (Lepidoptera: Noctuidae: Cuculliinae) and Peridroma saucia (Hübner) (Lepidoptera: Noctuidae: Noctuinae), on eight species of cultivated plants. In laboratory and greenhouse choice assays, we tested adult preference for oviposition and larval preference at 1 and 24 h. Larval performance was measured in terms of survival to adulthood, length of larval period, and pupal weight. We found that both adult females and larvae actively choose their hosts and that the larval preference toward the hosts is related to the females’ preference in both herbivore species. However, the females and larvae did not preferentially select the host with the best larval performance, indicating that larval performance is not related to female or larval preference and that other selective pressures are influencing the choice of the host plant in these two species.     

Absence of Learning and Local Specialization on Host Plant Selection by <Emphasis Type="BoldItalic">Heliconius erato</Emphasis>

There is considerable interspecific variation in larval host plants (Passifloraceae) used among Heliconius erato (Lepidoptera: Nymphalidae) populations. This study evaluates the role of learning and the influence of interspecific variation in host plant attributes on such local specialization in H. erato host plant choices. Experiments were conducted under laboratory, insectary, and field conditions, with the two most widely used host plants in southern Brazil (Passiflora suberosa Linnaeus and Passiflora misera Humbold, Bonpland et Kunth). Larval feeding preference and induction were evaluated through choice tests for all instars. Oviposition was evaluated in relation to host plant preference, Hopkins host-selection principle, and conditioning time (for 3, 7, 11, or 15 days). Also, oviposition choice was tested regarding density, intemode length, and presence of intact terminal bud on P. suberosa and P. misera shoots. Both larvae and adults of H. erato phyllis showed preference for P. misera compared to P. suberosa, under all conditions. Larval feeding preference could not be induced for most instars. The Hopkins effect was not detected and oviposition choice could not be conditioned. Females alternated use of host plant species as a function of variation in either density or presence of terminal buds on shoots. Thus, our data indicate host plant preference in H. erato phyllis is not learned but innate. Therefore, we concluded that variation in local use of host plant by this butterfly in southern Brazil results from qualitative and quantitative variation of the passion vine species.     

Host-plant susceptibility to the carrot fly, Psila rosae. 1. Acceptability of various host species to ovipositing females

A preference hierarchy of the oligophagous carrot fly for 30 umbelliferous host-plant species or varieties and six non-hosts was assessed. Foliage of the test plants was presented to a laboratory population of the fly in oviposition choice experiments together with leaves of a standard plant, the susceptible carrot cultivar “Danvers”. Only two species (Anthriscus cerefolium, Carum carvi) were more acceptable than the standard plant, while about half the species received significantly fewer eggs. Some umbellifers (Anethum graveolens, Pimpinella major) had a low acceptability similar to that of non-hosts (non-umbelliferous plants). The results obtained with dual and multiple choice assays were in agreement. A multiple choice assay with potted plants yielded a similar ranking of the species as assays using detached leaves, indicating that foliage is representative for whole plants. Variability in the exploratory runs performed by the females on the leaves prior to egg-laying is described and quantified for hosts and non-hosts. Differences in post-alighting pre-ovipositional behaviour of the female flies on the leaves accounted for a major part of the variation recorded in egg-laying.     

Host feeding experience affects host plant odour preference of the polyphagous leafminer Liriomyza bryoniae

Herbivorous insects use highly specific volatiles or blends of volatiles characteristic to particular plant species to locate their host plants. Thus, data on olfactory preferences can be valuable in developing integrated pest management tools that deal with manipulation of pest insect behaviour. We examined host plant odour preferences of the tomato leafminer, Liriomyza bryoniae (Kaltenbach) (Diptera: Agromyzidae), which is an economically important agricultural pest widespread throughout Europe. The odour preferences of leafminers were tested in dependence of feeding experiences. We ranked host plant odours by their appeal to L. bryoniae based on two‐choice tests using a Y‐tube olfactometer with five host plants: tomato, Solanum lycopersicum Mill.; bittersweet, Solanum dulcamara L.; downy ground‐cherry, Physalis pubescens L. (all Solanaceae); white goosefoot, Chenopodium album L. (Chenopodiaceae); and dead nettle, Lamium album L. (Lamiaceae). The results imply that ranking of host plant odours by their attractiveness to L. bryoniae is complicated due to the influence of larval and adult feeding experiences. Without any feeding experience as an adult, L. bryoniae males showed a preference for the airflow with host plant odour vs. pure air, whereas females did not display a preference. Further tests revealed that adult feeding experience can alter the odour choice of L. bryoniae females. After feeding experience, females showed a preference for host plant odour vs. pure air. Feeding experience in the larval stage influenced the choice by adults of both sexes: for males as well as females reared on bittersweet the odour of that plant was the most attractive. Thus, host feeding experience both in larval and/or adult stage of polyphagous tomato leafminer L. bryoniae influences host plant odour preference by adults.     

PREFERENCE HIERARCHIES AND THE ORIGIN OF GEOGRAPHIC SPECIALIZATION IN HOST USE IN SWALLOWTAIL BUTTERFLIES

Four allopatric populations of the widely distributed western anise swallowtail butterfly, Papilio zelicaon, use different plant genera as hosts, but simultaneous choice experiments showed that these populations have diverged only slightly in oviposition preference. Of the four populations—two from southeastern Washington State, one from coastal southwestern Washington State, and one from central California—three use hosts that are not available to any of the others. Although variation for the degree of preference for particular plant species occurred within and among populations, all four populations ranked hosts in the same overall order. Monophagy on a local, low-ranking host outside the range of high-ranking hosts did not necessarily lead to the loss of preference for those high-ranking hosts, thereby indicating that the high-ranking hosts would still be accepted, and in some cases even preferred, if a population encountered them again. Hence, the overall preference hierarchy among P. zelicaon populations appears to be evolutionarily conservative. Analyses of differences among families within the California population indicated that increased preference for some hosts is inversely correlated, whereas preference for other hosts may be uncorrelated. Positive correlations may also occur but were not observed among the plant species tested. Overall, the results indicate local monophagy on different plant species in P. zelicaon has not involved major reorganizations in the preference hierarchy of ovipositing females, even in populations that may have fed on a low-ranking host for many generations. Instead, small increases in preference for local hosts have occurred within an evolutionarily conservative preference hierarchy.     

Phenological matching rather than genetic variation in host preference underlies geographical variation in host plants used by orange tip butterflies

An insect species that shows variation in host species association across its geographical range may do so either because of local adaptation in host plant preference of the insect or through environmentally or genetically induced differences in the plants, causing variation in host plant suitability between regions. In the present study, we experimentally investigate the host plant preference of Anthocharis cardamines (orange tip butterfly) in two populations from the UK and two from Sweden. Previous reports indicate that A. cardamines larvae are found on different host plant species in different regions of the UK, and some variation has been reported in Sweden. Host plant choice trials showed that females prefer to oviposit on plants in an earlier phenological stage, as well as on larger plants. When controlling for plant phenological stage and size, the host species had no statistically significant effect on the choice of the females. Moreover, there were no differences in host plant species preference among the four butterfly populations. Based on our experiment, the oviposition choice by A. cardamines mainly depends on the phenological stage and the size of the host plant. This finding supports the idea that the geographical patterns of host–plant association of A. cardamines in the UK and Sweden are consequences of the phenology and availability of the local hosts, rather than regional genetic differences in the host species preference of the butterfly.     

Host plant preference and performance of the vine weevil Otiorhynchus sulcatus

Abstract 1 The relationship between reproductive performance and preference for potential host plants of the vine weevil is investigated, as shown in tests on contact (or feeding) preference, presented herein, and tests on olfactory preference, published elsewhere. 2 Assessment of reproductive performance shows that the host‐plant range of the adult vine weevil Otiorhynchus sulcatus in Europe is limited to one gymnosperm genus (Taxus sp.) and a broad range of angiosperm plants in two subclasses of the Dicotyledonae, namely Dilleniidae and Rosidae. The successful reproduction on very distantly related plant taxa suggests that the original weevil‐ and plant‐habitat has mediated the current host‐plant range of the vine weevil. 3 Contact‐preference tests with equally suitable hosts, such as Aronia, Fragaria, Euonymus and Taxus, and one less suitable host, Humulus, indicate a mismatch between contact preference and performance and, as far as olfactory preferences are known, these match neither the contact preferences nor the performance. This mismatch may arise because (i) host plant species offered do not occur in weevil habitat in Europe (e.g. Aronia and the cultivated Fragaria come from North America) and (ii) predation (or disease) risks differ among host plants, thereby altering effective reproductive performance. 4 With respect to performance on novel hosts (Thuja, Prunus) and bad hosts (Rhododendron), some between‐individual variation is found within a single population, suggesting that local populations harbour (possibly genetic) variation for adaptation to new hosts. How this variation is maintained in the face of strong selection pressures on local populations of flightless and thelytokous weevils, is an important question for understanding the broad host plant range in the vine weevil.     

Diversification of host use in two polyphagous butterflies: differences in oviposition specificity or host rank hierarchy?

Novel host usage may represent an initial step towards diversification or radiation onto novel hosts within an evolutionary lineage, particularly if a shift in host plant preference ranking takes place. Polyphagous stages of evolutionary lineages may represent transitional states in which novel host associations are more likely to develop, but may be more difficult to detect experimentally. The polyphagous sister species Papilio glaucus L. and Papilio canadensis (Lepidoptera: Papilionidae; these Papilio = Pterourus) are known to exhibit differences in host‐plant use, despite significant overlap in host‐use abilities, providing an opportunity to examine how host shifts in polyphagous species may occur and what the implications for future divergence may be. In particular, we were interested in (i) determining whether differences in oviposition behavior of these species were due to changes in specificity or shifts in host‐plant hierarchy, (ii) whether the varying preference for primary hosts also affected the preference for secondary hosts, and (iii) what the oviposition preferences of a new hybrid swarm population are. We examined more than 40 000 oviposition bouts from more than 400 P. glaucus, P. canadensis, and hybrid females placed in seven‐, three‐, or two‐choice assays. In each of the choice assays, leaves from plants in different plant families of varying suitability for P. glaucus and P. canadensis larvae were used. We found the primary difference between P. glaucus and P. canadensis to be limited to a Z‐linked shift in host rank hierarchy due to an acceptance of Populus tremuloides Michx. (Salicaceae) and reduced specificity for Liriodendron tulipifera L. (Magnoliaceae) in P. canadensis. In addition, we found the absence of the Z‐linked oviposition acceptance of P. tremuloides in a recently formed allochronically separated hybrid swarm population found in P. canadensis territory at the northern border of the P. glaucus and P. canadensis hybrid zone.     

Genetic interactions influence host preference and performance in a plant-insect system

Phytophagous insects generally feed on a restricted range of host plants, using a number of different sensory and behavioural mechanisms to locate and recognize their host plants. Phloem-feeding aphids have been shown to exhibit genetic variation for host preference of different plant species and genetic variation within a plant species can also have an effect on aphid preference and acceptance. It is known that genotypic interactions between barley genotypes and Sitobion avenae aphid genotypes influence aphid fitness, but it is unknown if these different aphid genotypes exhibit active host choice (preference) for the different barley genotypes. Active host choice by aphid genotypes for particular plant genotypes would lead to assortative association (non-random association) between the different aphid and plant genotypes. The performance of each aphid genotype on the plant genotypes also has the ability to enhance these interactions, especially if the aphid genotypes choose the plant genotype that also infers the greatest fitness. In this study, we demonstrate that different aphid genotypes exhibit differential preference and performance for different barley genotypes. Three out of four aphid genotypes exhibited preference for (or against) particular barley genotypes that were not concordant with differences in their reproductive rate on the specific barley genotype. This suggests active host choice of aphids is the primary mechanism for the observed pattern of non-random associations between aphid and barley genotypes. In a community context, such genetic associations between the aphids and barley can lead to population-level changes within the aphid species. These interactions may also have evolutionary effects on the surrounding interacting community, especially in ecosystems of limited species and genetic diversity.     

Drought stress drives intraspecific choice of food plants by Atta leaf‐cutting ants

Leaf‐cutting ants (LCA) are polyphagous and dominant herbivores throughout the Neotropics that carefully select plant individuals or plant parts to feed their symbiotic fungus. Although many species‐specific leaf traits have been identified as criteria for the choice of food plants, the factors driving intraspecific herbivory patterns in LCA are less well studied. Herein, we evaluate whether or not drought‐stressed native plants are a preferred food source using free‐living colonies of two leaf‐cutting ants, Atta sexdens L. (Hymenoptera: Formicidae: Attini), in combination with five plant species, Ocotea glomerata Nees (Lauraceae), Lecythis lurida S. A. Mori (Lecythidaceae), Miconia prasina DC (Melastomataceae), Tovomita brevistaminea Engl. (Clusiaceae), and Tapirira guianensis Aubl. (Anacardiaceae), and Atta cephalotes L., in combination with two plant species, O. glomerata and Licania tomentosa Benth. (Chrysobalanaceae). In dual‐choice bioassays, ants removed about three times more leaf area from drought‐stressed plants compared to control plants. Both leaf‐cutting ant species consistently preferred drought‐stressed plants for all species tested, except T. guianensis. The mean acceptability index – expressing the preference for one of two options on a scale of 0 to 1 – of drought‐stressed plants ranged from 0.65 to 0.86 across plant species, and the preference did not differ significantly among the tested plant species. Our results suggest that selection of drought‐stressed individuals is a general feature of food plant choice by leaf‐cutting ants irrespective of ant or plant species. As human‐modified forest assemblages across the Neotropics are increasingly prone to drought stress, the documented preference of Atta for drought‐stressed plants may have tangible ecological implications.     

Evolutionary conservatism of oviposition preference in a widespread polyphagous insect herbivore, Papilio zelicaon

We analyzed geographic differentiation in oviposition preference in the anise swallowtail butterfly, Papilio zelicaon Lucas, which is one of the most widely distributed and polyphagous butterflies in western North America. Among 13 populations that span 1200 km of the range of P. zelicaon in the Pacific Northwest of North America, the overall oviposition preference hierarchy has not diverged significantly, even though these populations differ in the plant species they use in the field. The results indicate that differences in host availability and use have not favored major reorganizations in the preference hierarchy of ovipositing females. Instead, this butterfly has a conserved preference hierarchy that varies within a narrow range among populations. All populations ranked the four test plant species in the same overall relative order, even though these populations differ in the plant species they use in the field. Received: 9 February 1996 / Accepted: 24 February 1997     

‘Do you remember the first time?’ Host plant preference in a moth is modulated by experiences during larval feeding and adult mating

In insects, like in other animals, experience‐based modulation of preference, a form of phenotypic plasticity, is common in heterogeneous environments. However, the role of multiple fitness‐relevant experiences on insect preference remains largely unexplored. For the multivoltine polyphagous moth Spodoptera littoralis we investigated effects of larval and adult experiences on subsequent reproductive behaviours. We demonstrate, for the first time in male and female insects, that mating experience on a plant modulates plant preference in subsequent reproductive behaviours, whereas exposure to the plant alone or plant together with sex pheromone does not affect this preference. When including larval feeding experiences, we found that both larval rearing and adult mating experiences modulate host plant preference. These findings represent the first evidence that host plant preferences in polyphagous insects are determined by a combination of innate preferences modulated by sensory feedback triggered by multiple rewarding experiences throughout their lifetime.     

Divergent host plant adaptation drives the evolution of sexual isolation in the grasshopper Hesperotettix viridis (Orthoptera: Acrididae) in the absence of reinforcement

Early stages of lineage divergence in insect herbivores are often related to shifts in host plant use and divergence in mating capabilities, which may lead to sexual isolation of populations of herbivorous insects. We examined host preferences, degree of differentiation in mate choice, and divergence in cuticular morphology using near‐infrared spectroscopy in the grasshopper Hesperotettix viridis aiming to understand lineage divergence. In Kansas (USA), H. viridis is an oligophagous species feeding on Gutierrezia and Solidago host species. To identify incipient mechanisms of lineage divergence and isolation, we compared host choice, mate choice, and phenotypic divergence among natural grasshopper populations in zones of contact with populations encountering only one of the host species. A significant host‐based preference from the two host groups was detected in host‐paired feeding preference studies. No‐choice mate selection experiments revealed a preference for individuals collected from the same host species independent of geographic location, and little mating was observed between individuals collected from different host species. Female mate choice tests between males from the two host species resulted in 100% fidelity with respect to host use. Significant differentiation in colour and cuticular composition of individuals from different host plants was observed, which correlated positively with host choice and mate choice. No evidence for reinforcement in the zone of contact was detected, suggesting that divergent selection for host plant use promotes sexual isolation in this species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 866–878.