Local adaptation and ecological genetics of host-plant specialization in a leaf beetle

The tendency of insect species to evolve specialization to one or a few plant species is probably a major reason for the remarkable diversity of herbivorous insects. The suggested explanations for this general trend toward specialization include a range of evolutionary mechanisms, whose relative importance is debated. Here we address two potentially important mechanisms: (i) how variation in the geographic distribution of host use may lead to the evolution of local adaptation and specialization; (ii) how selection for specialization may lead to the evolution of trade‐offs in performance between different hosts. We performed a quantitative genetic experiment of larval performance in three different populations of the alpine leaf beetle Oreina elongata reared on two of its main host plants. Due to differences in host availability, each population represents a distinctly different selective regime in terms of host use including selection for specialization on one or the other host as well as selection for utilizing both hosts during the larval stage. The results suggest that selection for specialization has lead to some degree of local adaptations in host use: both single‐host population had higher larval growth rate on their respective native host plant genus, while there was no difference between plant treatments in the two‐host population. However, differences between host plant treatments within populations were generally small and the degree of local adaptation in performance traits seems to be relatively limited. Genetic correlations in performance traits between the hosts ranged from zero in the two‐host population to significantly positive in the single‐host populations. This suggests that selection for specialization in single host populations typically also increased performance on the alternative host that is not naturally encountered. Moreover, the lack of a positive genetic correlation in the two host‐population give support for the hypothesis that performance trade‐offs between two host plants may typically evolve when a population have adapted to both these plants. We conclude that although there is selection for specialization in larval performance traits it seems as if the genetic architecture of these traits have limited the divergence between populations in relative performance on the two hosts.     

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.     

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.     

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.     

Counter-intuitive developmental plasticity induced by host quality

Adaptation to different hosts plays a central role in the evolution of specialization and speciation in phytophagous insects and parasites, and our ability to experimentally rank hosts by their quality is critical to research to understand these processes. Here we provide a counter-intuitive example in which growth is faster on poor quality hosts. The leaf beetles Oreina elongata and Oreina cacaliae share their host plant with the rust Uromyces cacaliae. Larvae reared on infected Adenostyles alliariae show reduced growth rate, reduced maximum weight and longer development time. However, they normally respond adaptively to the rust's mid-season arrival. When switched during development from healthy to infected leaves, larvae accelerate growth and reduce development time, but pupate at lower body weight. In this novel plant-insect-fungus interaction, infection forms the cue to trade off life-history traits in order to complete development within the brief alpine summer. It represents a novel mode of developmental plasticity, which is likely to be found in other host-parasite systems whenever host quality deteriorates due to multiple infection or ageing. This phenotypic plasticity would modify competition after co-infection and the mutual selection imposed by hosts and parasites, and creates a paradoxical negative correlation between growth rate and environmental quality.     

Host selection in phytophagous insects: a new explanation for learning in adults

Insect learning can change the preferences an egg laying female displays towards different host plant species. Current hypotheses propose that learning may be advantageous in adult host selection behaviour through improved recognition, accuracy or selectivity in foraging. In this paper, we present a hypothesis for when learning can be advantageous without such improvements in adult host foraging. Specifically, that learning can be an advantageous strategy for egg laying females when larvae must feed on more than one plant in order to complete development, if the fitness of larvae is reduced when they switch to a different host species. Here, larvae benefit from developing on the most abundant host species, which is the most likely choice of host for an adult insect which increases its preference for a host species through learning. The hypothesis is formalised with a mathematical model and we provide evidence from studies on the behavioural ecology of a number of insect species which demonstrate that the assumptions of this hypothesis may frequently be fulfilled in nature. We discuss how multiple mechanisms may convey advantages in insect learning and that benefits to larval development, which have so far been overlooked, should be considered in explanations for the widespread occurrence of learning.     

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.     

Glacial survival and local adaptation in an alpine leaf beetle

The challenge in defining conservation units so that they represent evolutionary entities has been to combine both genetic properties and ecological significance. Here we make use of the complexity of the European Alps, with their genetic landscape shaped by geographical barriers and postglacial colonization, to examine the correlation between ecological and genetic divergence. Montane species, because of the fragmentation of their present habitat, constitute extreme cases in which to test if genetically distinct subgroups based on neutral markers are also ecologically differentiated and show local adaptation. In the leaf beetle Oreina elongata, populations show variation in host plant use and a patchy distribution throughout the Alps and Apennines. We demonstrate that despite very strong genetic isolation (F(ST) = 0.381), variation in host plant use has led to differences in larval life-history traits between populations only as a secondary effect of host defence chemistry, and not through physiological adaptation to plant nutritional value. We also establish that populations that are more ecologically different in terms of larval performance are also more genetically divergent. In addition, morphological variation used to define subspecies appears to be mirrored in the population genetics of this species, resulting in almost perfect clustering based on microsatellite data. Finally, we argue from their strong genetic structure and congruent distribution that the subspecies of O. elongata were divided among the same glacial refugia within the Alps that have been proposed for alpine plants.     

Host plant finding in phytophagous insects: the case of the Colorado potato beetle

A short critical review is given on the literature of host plant finding in phytophagous insects with main emphasis on the Colorado potato beetle (Leptinotarsa decemlineata Say, col.: Chrysomelidae). The literature data are compared with the results of field experiments: (1) the foraging behaviour of adults was observed in a field arena on bare ground, and (2) adults were released in closed plant stands and recaptured by potted potato plants. It is concluded that host plant finding is a chance event in this species. The observed high directionality of move must be an adaptation increasing probability of host finding. Implications on population dynamics and agricultural practice are discussed.     

The significance of bottom-up effects for host plant specialization in Chrysomela leaf beetles

The leaf beetle species Chrysomela lapponica, which belongs to the so‐called C. interrupta group, forms distinct allopatric populations either on willows (Salicaceae) or birches (Betulaceae). It was recently suggested that, on several occasions, host plant shifts from Salicaceae to Betulaceae occurred independently within the C. interrupta group. Our study aims to elucidate bottom‐up effects of the host plants that might have shaped the evolution of host plant specialization in the populations of C. lapponica, and thus, to shed some light on the driving forces of host shifts within the C. interrupta group, too. We compared the oviposition behaviour and performance of two C. lapponica populations, one of which has adapted to birches and the other to willows. The studies were conducted under laboratory conditions, eliminating the impact of natural enemies. Experiments involving the transfer of individuals of the birch‐specialized population to willows and vice versa with individuals of the willow‐specialized population to birches aimed to examine the plasticity in host plant use. Females of each population almost exclusively chose their natural host plant for oviposition, when offering birch and willow in dual choice experiments. When specimens of the two C. lapponica populations were reared on their natural host plants, the birch specialists suffered higher mortality, needed a longer period of development and produced less larval defensive secretion than the willow specialists. When the birch specialists were fed with willow, these performance parameters decreased even more. Other parameters, such as body weight and fecundity, did not differ between birch and willow specialists when they were fed with their natural host plant. While individuals of the birch‐specialized population could be reared on willow, all neonate larvae from the willow‐specialized population died after being transferred to birch. The significance of these bottom‐up effects for the evolution of host plant specialization in C. lapponica is discussed.     

Do caterpillars disperse their damage?: larval foraging behaviour of two specialist herbivores,Euphydryas phaeton (Nymphalidae) and Pieris rapae (Pieridae)

Abstract. 1. To examine ecological and evolutionary aspects of caterpillar foraging behaviour, this study focused on observation of the individual foraging behaviour of two lepidopteran species, Pieris rapae L. and Euphydryas phaeton (Drury), on their respective host plants.
2. Periodic observations over the course of a day showed that the larvae move considerable distances, forage on the upper surfaces of leaves, and often immediately leave areas from which they have fed, leaving a pattern of dispersed herbivory.
3. Differences in foraging behaviour were not found between the two species, even though one species is aposematic and the other is cryptically coloured, but there were significant differences in the foraging patterns of P.rapae on the two host plants, broccoli and radish.     

Similarity and specialization of the larval versus adult diet of European butterflies and moths

Many herbivorous insects feed on plant tissues as larvae but use other resources as adults. Adult nectar feeding is an important component of the diet of many adult herbivores, but few studies have compared adult and larval feeding for broad groups of insects. We compiled a data set of larval host use and adult nectar sources for 995 butterfly and moth species (Lepidoptera) in central Europe. Using a phylogenetic generalized least squares approach, we found that those Lepidoptera that fed on a wide range of plant species as larvae were also nectar feeding on a wide range of plant species as adults. Lepidoptera that lack functional mouthparts as adults used more plant species as larval hosts, on average, than did Lepidoptera with adult mouthparts. We found that 54% of Lepidoptera include their larval host as a nectar source. By creating null models that described the similarity between larval and adult nectar sources, we furthermore showed that Lepidoptera nectar feed on their larval host more than would be expected if they fed at random on available nectar sources. Despite nutritional differences between plant tissue and nectar, we show that there are similarities between adult and larval feeding in Lepidoptera. This suggests that either behavioral or digestive constraints are retained throughout the life cycle of holometabolous herbivores, which affects host breadth and identity.     

Implications of a temperature increase for host plant range: predictions for a butterfly

Although changes in phenology and species associations are relatively well‐documented responses to global warming, the potential interactions between these phenomena are less well understood. In this study, we investigate the interactions between temperature, phenology (in terms of seasonal timing of larval growth) and host plant use in the polyphagous butterfly Polygonia c‐album. We found that the hierarchy of larval performance on three natural host plants was not modified by a temperature increase as such. However, larval performance on each host plant and temperature treatment was affected by rearing season. Even though larvae performed better at the higher temperature regardless of the time of the rearing, relative differences between host plants changed with the season. For larvae reared late in the season, performance was always better on the herbaceous plant than on the woody plants. In this species, it is likely that a prolonged warming will lead to a shift from univoltinism to bivoltinism. The demonstrated interaction between host plant suitability and season means that such a shift is likely to lead to a shift in selective regime, favoring specialization on the herbaceous host. Based on our result, we suggest that host range evolution in response to temperature increase would in this species be highly contingent on whether the population undergoes a predicted shift from one to two generations. We discuss the effect of global warming on species associations and the outcome of asynchrony in rates of phenological change.     

Natural selection in the laboratory for a change in resistance byDrosophila melanogaster to the parasitoid waspAsobara tabida

The selection response of the polymorphic hostD. melanogaster (Meigen) to the braconid waspA. tabida (Nees) is addressed. Cages of flies with and without wasps were initiated with a population ofD. melanogaster that exhibited variation both in larval foraging behavior and in encapsulation ability. Encapsulation ability was measured as the proportion of parasitized larvae that produce a hardened capsule which encapsulates the wasp egg and ultimately kills the wasp larva. We determined whether the host population changed its encapsulation ability and/or its foraging behavior in response to the wasp. Both species were collected from a local orchard whereA. tabida is the only wasp known to parasitizeD. melanogaster larvae. The naturally occurring genetic polymorphism for rover and sitter larval foraging behavior inD. melanogaster is also found in this field population.A. tabida's vibrotactic search behavior enables it to detect rover more frequently than sitter larvae. Rover larvae move significantly more while feeding than do sitter larvae. In this field population, rover larvae also show higher encapsulation abilities than do sitter larvae. Six cage populations, three without wasps and three with wasps, each containing an equal mixture of rover and sitter flies, were established in the laboratory and maintained for 19 fly generations. Selection pressure in the laboratory was similar to that found in the field population from which the flies and wasps were derived. We found that larvae from cages with wasps developed a significantly higher frequency of encapsulation than those reared without wasps. We were, however, unable to detect a change in larval movement (rover or sitter behavior) in larvae from cages subject to selection from wasps compared to larvae from cages containing no wasps. This may have resulted from a balance between two selective forces, selection against rovers by the wasps' use of vibrotaxis, and selection for rovers resulting from their increased encapsulation abilities     

The influence of host plant diversity and food quality on larval survival of plant feeding heteropteran bugs

Abstract. 1. In a laboratory experiment, the influence of host plant diversity and food quality, in terms of nitrogen content, on the larval survival of two oligophagous bug species (Heteroptera, Miridae: Leptopterna dolobrata L., Notostira erratica L.) was investigated. Both species are strictly phytophagous and capable of feeding on a wide range of grass species. Moreover, they typically change their host plants during ontogenesis; it has been suggested that this behaviour is a response to the changing protein content of the hosts.
2. To investigate the importance of host plant diversity for these insects, the development of insects reared on grass monocultures was compared with that on mixtures of four grass species. In addition, the host grasses were grown under two nitrogen regimes to test whether nitrogen content is the key factor determining host plant switching.
3. Both species had a significantly higher survival rate when feeding on several host plants but only L. dolobrata showed a significant response to food nitrogen content. Furthermore, there was no correlation between the nitrogen content of the host plants and the survival rate of N. erratica larvae.
4. The study suggests that at least some Stenodemini need a variety of host plants during larval development but that the level of host plant nitrogen is not the main factor responsible for the observed diversity effect.     

Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment

Plant chemical defenses and escape from natural enemies have been postulated to select for dietary specialization in herbivorous insects. In field and laboratory bioassays, we evaluated the effectiveness of intact and chemically modified larval shield defenses of the generalist Chelymorpha alternans and the specialists Acromis sparsa and Stolas plagiata (Chrysomelidae: Cassidinae) against three natural predators, using larvae reared on two morning glory (Convolvulaceae) species. We assessed whether: (1) specialists were better defended than generalists when both were fed and assayed on the same plant; (2) larval shield defenses were chemical, physical, or both; and (3) specialists exploit chemistry better than generalists. Live specialist larvae survived at higher rates than did generalists in predator bioassays with the bug Montina nigripes (Reduviidae), but there were no differences among groups against two species of Azteca ants (Hymenoptera: Dolichoderinae). Solvent leaching by H₂O or MeOH significantly reduced shield efficacy for all species compared to larvae with intact shields. In contrast, freshly killed specialist larvae exhibited significantly lower capture rates and frequencies than the generalists. Although solvent leaching significantly reduced overall shield efficacy for freshly killed larvae of all species, the pattern of leaching effects differed between specialists and generalists, with H₂O-leaching having a greater impact on the specialists. The overall vulnerability of the generalists appears due to lower chemical protection, which is ameliorated by increased escape behaviors, suggesting a selective trade-off between these defensive components. These experiments indicate that shield defenses are essential for larval survival and that specialists are superior at exploiting plant compounds residing in the aqueous fraction. Our results support the hypothesis that diet-specialized herbivorous insects have more effective defenses than generalists when both feed on the same plant due to the differential ability to exploit defensive precursors obtained from the host. The evolution of dietary specialization may therefore confer the advantage of enhanced enemy-free space.     

Host specialization involving attraction,avoidance and performance,in two phytophagous moth species

Host specialization plays a key role in the extreme diversification of phytophagous insects. Whereas proximate mechanisms of specialization have been studied extensively, their consequences for species divergence remain unclear. Preference for, and performance on hosts are thought to be a major source of divergence in phytophagous insects. We assessed these major components of specialization in two moth species, the European corn borer (ECB) and the Adzuki bean borer (ABB), by testing their oviposition behaviour in different conditions (choice or no‐choice set‐ups) and their performances, by reciprocal transplant at the larval stage on the usual host and an alternative host plant. We demonstrated that both ABB and ECB have a strong preference for their host plants for oviposition, but that relative larval performances on the usual host and an alternative host differed according to the experiment and the trait considered (weight or survival). Finally, we show for the first time that the preference for maize in ECB conceals a strong avoidance of mugwort. The differences in performance, attraction and avoidance between ECB and ABB are discussed in the light of the underlying mechanisms and divergence process.     

Does ant predation favour leaf beetle specialization on toxic host plants?

Generalist predators are frequently seen as evolutionary forces that narrow the host range in herbivorous insects. Predators may favour specialization of herbivores on host plants containing toxic chemicals (which can be used by herbivores for their own defence) if host plant‐derived defences provide better protection from enemies than do autogenously produced defences. We compared the effectiveness of these two defensive strategies in the larvae of six species of leaf beetle (Chrysomelidae) against wood ants (Formica rufa group) in field experiments. Ants were more strongly repelled by larvae with host plant‐derived, salicylaldehyde‐containing secretions than by larvae with various autogenous secretions, but collectively foraging ants ultimately overcame any type of chemical defence by social interactions, chemical signalling, and olfactory learning. As a result, ants killed all larvae of Chrysomela lapponica defended by salicylaldehyde‐containing secretions within 2 days of their introduction to willows within 15 m of ant nests. We conclude that in the field neither type of chemical defence provides complete protection against wood ants in the vicinity of their nests, and that evolutionary shifts from autogenous production of secretion to sequestration of plant allelochemicals in leaf beetles may be favoured mostly at low ant densities on the periphery of ant foraging areas.     

Divergent host acceptance behavior suggests host specialization in populations of the polyphagous mite Abacarus hystrix (Acari: Prostigmata: Eriophyidae)

For phytophagous arthropods, host acceptance behavior is a key character responsible for host plant specialization. The grain rust mite, Abacarus hystrix (Nalepa), is an obligately phytophagous, polyphagous eriophyid mite recorded from at least 70 grass species. In this study, the hypothesis that two host populations of this mite (one collected from quackgrass and the other from ryegrass) are highly host-specific was tested using behavioral data. For this purpose, female behavior when exposed to familiar and novel host plants was observed in no-choice cross experiments. Altogether, 13 variables were used to describe mite behavior. Data were subjected to principal component analysis, and host acceptance behavior was subsequently tested with generalized estimating equations (GEE). Distinct variation in female behavior between familiar and novel hosts was observed. Females from neither population accepted novel hosts. This was recorded as significant differences in the occupation of and overall activity on particular plant parts. On their familiar host, females were not active and showed little tendency to move. On novel hosts females were more active and mobile, spending more time walking, running, and climbing on the whole plant surface and showing a tendency to disperse. Other differences in behavior between studied populations were also observed. Thus, the results suggest that mites of these two studied populations (1) differ in their behaviors during plant exploitation and (2) can quickly distinguish between their familiar host and an unfamiliar host used by a conspecific. These findings support the hypothesis of narrow host specialization of ryegrass and quackgrass populations of this highly polyphagous species.     

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.