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.     

Isolation and characterization of microsatellite loci in the Alpine leaf beetle,Oreina elongata

For a study of local adaptations in the Alpine leaf beetle, Oreina elongata, we developed six microsatellite loci and screened them in 305 individuals from 13 populations. All markers were polymorphic with three to 15 alleles per locus. Average observed and expected heterozygosity values were 0.14 and 0.62, respectively. Four markers showed heterozygote deficiency and deviated significantly from Hardy–Weinberg expectations, indicating the presence of null alleles.     

Evolutionary conservatism of geographic variation in host preference in Callosobruchus maculatus

Abstract.  1. A study of host preference of four pairs of populations of the cowpea weevil Callosobruchus maculates was carried out. The pairs had different geographical origins.
2. One population of each pair had been maintained for about 110 generations on cowpea Vigna unguiculata , the other population had been maintained on mung bean V. radiata . Half of the tested females from each population were raised on cowpea and exposed to this host prior to the assay; the other half was raised on mung bean. This design permitted assessment of the relative contributions of geographical origin, recent host use in the laboratory, and individual experience, to variation in host preference.
3. Host preference was assayed by letting the females oviposit on an equal-weight mixture of cowpea and mung seeds; two experiments were performed six generations apart.
4. Both experiments revealed a strong effect of geographical origin: populations originating from Nigeria laid a much greater proportion (68–86%) of their eggs on cowpea than those originating from Uganda and Yemen (30–42%); those from Cameroon were intermediate (56–60%). These preferences were not affected consistently by about 110 generations of laboratory evolution on one or the other host, or by experience of individual females.
5. These results indicate considerable geographical variation in host preference, and suggest that host preference is behaviourally inflexible and evolutionarily conserved.     

Host plant choice in the comma butterfly-larval choosiness may ameliorate effects of indiscriminate oviposition

In most phytophagous insects, the larval diet strongly affects future fitness and in species that do not feed on plant parts as adults, larval diet is the main source of nitrogen. In many of these insect-host plant systems, the immature larvae are considered to be fully dependent on the choice of the mothers, who, in turn, possess a highly developed host recognition system. This circumstance allows for a potential mother-offspring conflict, resulting in the female maximizing her fecundity at the expense of larval performance on suboptimal hosts. In two experiments, we aimed to investigate this relationship in the polyphagous comma butterfly, Polygonia c-album, by comparing the relative acceptance of low- and medium-ranked hosts between females and neonate larvae both within individuals between life stages, and between mothers and their offspring. The study shows a variation between females in oviposition acceptance of low-ranked hosts, and that the degree of acceptance in the mothers correlates with the probability of acceptance of the same host in the larvae. We also found a negative relationship between stages within individuals as there was a higher acceptance of lower ranked hosts in females who had abandoned said host as a larva. Notably, however, neonate larvae of the comma butterfly did not unconditionally accept to feed from the least favorable host species even when it was the only food source. Our results suggest the possibility that the disadvantages associated with a generalist oviposition strategy can be decreased by larval participation in host plant choice.     

Response of the elm leaf beetle to host plants induced by oviposition and feeding: the infestation rate matters

We investigated by olfactometry and feeding‐ and oviposition‐choice‐tests how the highly specialised elm leaf beetle, Xanthogaleruca luteola Müller (Coleoptera: Chrysomelidae), responds to conspecifically induced defences in the field elm Ulmus minor Miller (Ulmaceae). While egg deposition of the beetle induced elms to release volatiles attractive to the egg parasitoid Oomyzus gallerucae Fonscolombe (Hymenoptera: Eulophidae), feeding alone did not. In the present study, females of the elm leaf beetle showed preferences for the odours of twigs induced by low egg deposition and feeding over odours from uninfested twigs. In contrast, heavy infestation rendered elm odours less attractive to the beetles. Feeding and oviposition bioassays revealed an oviposition preference for leaves from uninfested twigs when compared to locally infested leaves. However, beetles preferred to feed upon systemically induced leaves compared to uninfested ones. The different preferences of the elm leaf beetle during host plant approach might be explained by a strategy that accounts for both gaining access to high quality nutrition and avoiding competition or parasitism.     

Geographic variation of host use in the leaf beetle Agelasa nigriceps suggests host range expansion

Host range expansion is an important event in the evolution of host use in phytophagous insects. Herein, we report geographic variation of host use in the chrysomelid leaf beetle, Agelasa nigriceps Motschulsky (Coleoptera: Chrysomelidae), and suggest that this beetle is expanding its host range. This beetle has been recently recorded on Pterostyrax hispidus Sieb. et Zucc. (Styracaceae) in addition to its common host plant Actinidia arguta (Sieb. et Zucc.) Planch. ex Miq. (Actinidiaceae). The A. arguta‐associated populations were widely found in Japan, whereas the P. hispidus‐associated populations were found only in central and southwestern Japan. In the present study, we examined adult feeding behavior and larval performance of 12 A. nigriceps populations collected from eight localities, four localities where beetles occurred only on A. arguta (allopatric localities) and four localities where A. arguta‐ and P. hispidus‐associated populations occurred sympatrically (sympatric localities). Beetles of all populations, irrespective of their host plants and localities, showed high acceptance of and high larval performance on A. arguta leaves. In contrast, we found considerable variation in the beetle response to P. hispidus leaves. The A. arguta‐associated populations of allopatric localities scarcely accepted P. hispidus leaves, whereas those of sympatric localities, particularly those of P. hispidus‐associated populations, accepted and grew on P. hispidus leaves, although the degree of acceptance and larval performance varied among localities. These results strongly suggest that A. arguta is the ancestral host for A. nigriceps, and host range expansion to the P. hispidus has occurred in this beetle.     

An alternative hibernation strategy involving sun-exposed 'hotspots', dispersal by flight, and host plant finding by olfaction in an alpine leaf beetle

Oreina cacaliae (Schrank) (Coleoptera: Chrysomelidae) has a 2‐year life cycle that it has to complete within the short warm seasons of the harsh alpine environment. Three years of field observations and experiments revealed that not all beetles overwintered in the soil next to their principal host Adenostyles alliariae (Asteraceae), as was previously assumed, but that many O. cacaliae left their host in autumn and flew to overwintering sites that were extensively sun‐exposed. In spring, these individuals became active 2 months earlier than their conspecifics that had remained in the soil close to the host plant. These early beetles flew from their hibernation sites against the direction of the prevailing wind. After a random landing in snow, they walked to the spring host Petasites paradoxus (Asteraceae) and fed on its floral stalks, the only plant parts present at that time. A few weeks later, they took flight again to locate newly emerging A. alliariae on which they would feed and deposit larvae as did individuals that had overwintered close to A. alliariae. Leaves of A. alliariae contain pyrrolizidine alkaloids (PAs), which the beetles sequester for their own defence. The dominating PA (seneciphylline) was also found to be present in the floral stalks of P. paradoxus. With additional behavioural assays in the field and laboratory, we demonstrated the importance of plant odours in the short‐range host location process. This study reveals a unique hibernation behaviour in which part of the beetle population uses exceptionally warm locations from which they emerge in spring, long before all the snow has melted. This early, but risky emergence allows them to exploit a second, highly suitable host plant, which they locate first by wind‐guided flight and then by odour‐guided walking. The well‐fed beetles then use odour again to move to their principal host plant, on which they reproduce.     

Temporal and host-related variation in frequencies of genes that enable Phyllotreta nemorum to utilize a novel host plant, Barbarea vulgaris

The flea beetle, Phyllotreta nemorum L. (Coleoptera: Chrysomelidae), is an intermediate specialist feeding on a small number of plants within the family Brassicaceae. The most commonly used host plant is Sinapis arvensis L., whereas the species is found more rarely on Cardaria draba (L.) Desv., Barbarea vulgaris R.Br., and cultivated radish (Raphanus sativus L.). The interaction between flea beetles and Barbarea vulgaris ssp. arcuata (Opiz.) Simkovics seems to offer a good opportunity for experimental studies of coevolution. The plant is polymorphic, as it contains one type (the P‐type) that is susceptible to all flea beetle genotypes, and another type (the G‐type) that is resistant to some genotypes. At the same time, the flea beetle is also polymorphic, as some genotypes can utilize the G‐type whereas others cannot. The ability to utilize the G‐type of B. vulgaris ssp. arcuata is controlled by major dominant genes (R‐genes). The present investigation measured the frequencies of flea beetles with R‐genes in populations living on different host plants in 2 years (1999 and 2003). Frequencies of beetles with R‐genes were high in populations living on the G‐type of B. vulgaris ssp. arcuata in both years. Frequencies of beetles with R‐genes were lower in populations living on other host plants, and declining frequencies were observed in five out of six populations living on S. arvensis. Selection in favour of R‐genes in populations living on B. vulgaris is the most likely mechanism to account for the observed differences in the relative abundance of R‐genes in flea beetle populations utilizing different host plants. A geographic mosaic with differential levels of interactions between flea beetles and their host plants was demonstrated.     

The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle

The genetic basis of host plant use by phytophagous insects can provide insight into the evolution of ecological niches, especially phenomena such as specialization and phylogenetic conservatism. We carried out a quantitative genetic analysis of multiple host use traits, estimated on five species of host plants, in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Mean values of all characters varied among host plants, providing evidence that adaptation to plants may require evolution of both behavioral (preference) and post-ingestive physiological (performance) characteristics. Significant additive genetic variation was detected for several characters on several hosts, but not in the capacity to use the two major hosts, a pattern that might be caused by directional selection. No negative genetic correlations across hosts were detected for any 'performance' traits, i.e. we found no evidence of trade-offs in fitness on different plants. Larval consumption was positively genetically correlated across host plants, suggesting that diet generalization might evolve as a distinct trait, rather than by independent evolution of feeding responses to each plant species, but several other traits did not show this pattern. We explored genetic correlations among traits expressed on a given plant species, in a first effort to shed light on the number of independent traits that may evolve in response to selection for host-plant utilization. Most traits were not correlated with each other, implying that adaptation to a novel potential host could be a complex, multidimensional 'character' that might constrain adaptation and contribute to the pronounced ecological specialization and the phylogenetic niche conservatism that characterize many clades of phytophagous 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.     

Nitrogen homeostasis in a willow leaf beetle, Plagiodera versicolora, is independent of host plant quality

While foliar nitrogen (N) content of host plants depends on environmental conditions, N content of herbivorous insects may remain relatively constant due to homeostasis. However, it is unknown to what extent insects can maintain their body elemental composition against natural variation in host plant quality. The present study examined the performance and N content of a willow leaf beetle, Plagiodera versicolora Laicharting (Coleoptera: Chrysomelidae), when fed leaves of host willow, Salix eriocarpa Franchet et Savatier (Salicaceae), with varying nutritional status. Water content, toughness, and N content of willow leaves varied seasonally, and they affected performance of the leaf beetle. The leaf beetle achieved high performance when fed young leaves. On the other hand, the N content of the leaf beetle changed little, and it was independent of that of willow leaves, indicating strong N homeostasis of the leaf beetle. We discussed the function of N homeostasis in herbivorous insects in tritrophic level interactions.     

Effects of leaf pubescence in Salix borealis on host- plant choice and feeding behaviour of the leaf beetle, Melasoma lapponica

Density of leaf trichomes in Salix borealis affected both the choice of individual host plants and feeding behaviour of adults and last instar larvae of the willow feeding leaf beetle, Melasoma lapponica. Beetles clearly preferred shaved disks to unshaved ones taken from the same leaf; this preference was highest in leaves of the most pubescent plants. High leaf pubescence explained the low preference for willow clones from the high density site in among-site preference trials; shaving significantly increased the consumption of these pubescent willow clones. In no-choice experiments, the food consumption by both adults and last instar larvae decreased with an increase in leaf pubescence. The time budget of adults did not depend on leaf pubescence of the host plants, however adults compelled to feed on highly pubescent plants changed their feeding sites twice as often as on less pubescent willow clones. Larvae feeding on highly pubescent plants spend moving three times as much time as larvae feeding on less pubescent plants. Combined with our earlier observations on the increase in leaf pubescence in the year(s) following defoliation, these data suggest that leaf hairiness may have contributed to the delayed induced resistance in S. borealis by disturbing the feeding behaviour of M. lapponica.     

Plant resistance, plant traits, and host plant choice of the leaf-folding sawfly on the arroyo willow

Abstract. 1. The hypotheses that genetic variation in host plant resistance of the arroyo willow affected leaf folder ( Phyllocolpa sp.) (Hymenoptera: Tenthredinidae) density and that genetic variation in shoot length and leaf length was correlated with resistance were tested.
2. Willows grown in pots and exposed to ovipojsition by the leaf folding sawfly in cages had significantly different densities among clones, indicating variation in resistance caused by genetic differences among conspecific host plants.
3. There was a general correspondence between leaf folder density on potted cuttings and on the plants in the field that were the sources of cuttings.
4. In behavioural choice experiments, susceptible clones (with highest leaf fold densities) had the highest oviposition activity of female leaf folders compared to clones that were resistant to the leaf folder.
5. Clones differed significantly in shoot length and leaf length among clones grown in pots, among clones in the field, and between shoots with galls and shoots without galls on clones in the field.
6. Leaf folder density was significantly positively correlated with mean shoot length on field clones in 1985 and 1986, but was not correlated with leaf length, although leaf length and shoot length were correlated.
7. Leaf length variation among willow clones accounted for a significant portion of the variation in resistance of potted willows, but shoot length was unimportant.     

The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis

1. A series of experiments was conducted to measure the impact of plant genotype, plant growth rate, and intraspecific competition on the oviposition preference and offspring performance of the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and Solidago gigantea (Asteraceae). Previous research has shown that both host races prefer to oviposit on their own host plant where survival is much higher than on the alternate host plant. In this study, neither host race showed any relationship between oviposition preference and offspring performance in choosing among plants of their natal host species. 2. The larval survival of both host races differed among plant genotypes when each host race oviposited on its natal host species. In one experiment, altissima host race females showed a preference among plant genotypes that was not correlated with offspring performance on those genotypes. In all other experiments, neither the altissima nor gigantea host race demonstrated a preference for specific host plant genotypes. 3. Eurosta solidaginis had a preference for ovipositing on rapidly growing ramets in all experiments, however larval survival was not correlated with ramet growth rate at the time of oviposition. 4. Eurosta solidaginis suffered high mortality from intraspecific competition in the early larval stage. There was little evidence, however, that females avoided ovipositing on ramets that had been attacked previously. This led to an aggregated distribution of eggs among ramets and strong intraspecific competition. 5. There was no interaction among plant genotype, plant growth rate, or intraspecific competition in determining oviposition preference or offspring performance.     

Phenotypic plasticity in host plant preference of the willow leaf beetle Phratora vulgatissima: the impact of experience made by adults

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Oviposition site selection on oats: the effect of plant architecture,plant and leaf age,tissue toughness,and hardness on cereal leaf beetle,Oulema melanopus

In sequentially planted oat stands, the cereal leaf beetle (CLB), Oulema melanopus (L.) (Coleoptera: Chrysomelidae: Lemini), is found in greater numbers, and lays more eggs, on later planted (younger) oats (Avena sativa L.) (Poaceae). Plant characteristics that could explain this ovipositional preference were examined in a series of experiments. Cage and open field whole plant preference tests confirmed the attraction of ovipositing females to younger oats. A cage effect illustrated the role of plant architecture (plant height) in CLB host selection. Two multiple‐choice and one no‐choice excised leaf experiments determined that characteristics of individual leaves associated with leaf insertion level (leaf number from base to apex) and age influence ovipositional site selection. Leaves of higher insertion level have higher nitrogen content, but fewer eggs are laid on those leaves. Two experiments examining the interaction between total leaf nitrogen and leaf insertion level showed that only leaf insertion level affected oviposition choice. Published literature suggests variation in secondary plant compounds cannot explain O. melanopus ovipositional preference among leaves. Grass leaves of higher insertion level have more extensively developed cells associated with tissue toughness and hardness. The data and supporting literature suggest tissue toughness and hardness are deterring oviposition on oat leaves of higher insertion level. However, newly eclosed larvae are able to feed on leaves usually avoided as oviposition sites. The explanation for this result may be a lack of correlation between host suitability and ovipositional preference.     

Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant

Much attention has been paid to ecology and evolution of damage-induced plant responses. Recently, it has been emphasized that phenotypic plasticity, such as induced plant responses, has the potential to lead to evolutionary changes of interacting partners. Here, we report that induced plant regrowth promotes a locally adaptive feeding preference of a leaf beetle, Plagiodera versicolora . We found that there was among-population variation in the strength of the feeding preference of the leaf beetle for leaf-age types of conspecific host plants. The strength of the preference was positively correlated to leaf production of host plants across populations, and the intensity of induced regrowth was likely to have been responsible for geographic variation in new leaf production. Within one population, we detected a significant additive genetic variance and heritability in the preference for consuming new vs. old leaves. Moreover, the strength of preference was significantly related to egg production depending on the leaf-age types. Thus, allopatric populations can evolutionarily develop different adaptive preference, according to locally distinct patterns of induced host regrowth.     

Oviposition strategy as a means of local adaptation to plant defence in native and invasive populations of the viburnum leaf beetle

Herbivores have been hypothesized to adapt locally to variation in plant defences and such adaptation could facilitate novel associations in the context of biological invasions. Here, we show that in the native range of the viburnum leaf beetle (VLB, Pyrrhalta viburni), two populations of geographically isolated hosts-Viburnum opulus and Viburnum tinus-have divergent defences against VLB oviposition: negative versus positive density-dependent egg-crushing wound responses, respectively. Populations of beetles coexisting with each host show an adaptive behavioural response: aggregative versus non-aggregative oviposition on V. opulus and V. tinus, respectively. In parallel, we show that in North America, where VLB is invasive, defences of three novel hosts are negatively density-dependent, and beetles' oviposition behaviour is aggregative. Thus, local adaptation to plant defences has the potential to facilitate the invasion of herbivores onto novel hosts.     

Geographic variation in oviposition preference for male and female host plants in a geometrid moth: implications for evolution of host choice

Several dioecious plant species exhibit sexual dimorphisms in defensive traits. However, the effects of sexual dimorphism on defense against herbivores remain poorly understood. Eurya japonica (Thunb.) (Theaceae) is a dioecious shrub that shows sexual dimorphism in the chemical defense of flower buds. Female calyces contain higher concentrations of total phenolics and condensed tannins than do male calyces. Male flower buds are edible for a florivore moth, Chloroclystis excisa (Butler) (Lepidoptera: Geometridae), whereas the female flower buds are lethal to the moth larvae. The moths prefer to oviposit on male over female E. japonica flower buds. As the moths also occur in areas lacking E. japonica, we tested whether the oviposition preference for E. japonica flower sex differed between moths sympatric and allopatric with E. japonica. The moths sympatric with E. japonica showed a stronger preference for male E. japonica than the moths allopatric with E. japonica. Our phylogeographic study using mitochondrial cytochrome oxidase subunit I gene sequences revealed little genetic differentiation between moth populations sympatric and allopatric with E. japonica. These results suggest that the adaptive oviposition preference for flower sex of E. japonica has evolved rapidly in C. excisa.     

Non‐random segregation of an autosomal gene in males of the flea beetle,Phyllotreta nemorum: implications for colonization of a novel host plant

The flea beetle, Phyllotreta nemorum (L.) (Coleoptera: Chrysomelidae: Alticinae), is currently expanding its host plant range in Europe. The ability to utilize a novel host plant, Barbarea vulgaris R. Br. (Brassicaceae), is controlled by major dominant genes named R‐genes. The present study used extensive crossing experiments to illustrate a peculiar mode of inheritance of the R‐gene in a population from Delemont (Switzerland). When resistant males from Delemont are mated with recessive females from a laboratory line, the female F₁ offspring contains the R‐allele and is able to utilize B. vulgaris, whereas the male offspring contains the r‐allele and is unable to utilize the plant. This outcome suggests X‐linkage of the R‐gene, but further crossing experiments demonstrated that this was not the case. When the R‐gene is present in offspring from males from a laboratory line that originates from Taastrup (Denmark), it is transmitted to female and male offspring in equal proportions as a normal autosomal gene. The results demonstrate a polymorphism in segregation patterns of an autosomal R‐gene in P. nemorum males. Males from Delemont contain a factor which causes non‐random segregation of the R‐gene (NRS‐factor). This factor is inherited patrilineally (from fathers to sons). Males with the NRS‐factor transmit the R‐gene to their female offspring, whereas males without the NRS‐factor transmit the R‐gene to female and male offspring in equal proportions. Various models for the non‐random segregation of autosomes in P. nemorum males are discussed – e.g., fusions between autosomes and sex chromosomes, and genomic imprinting. The implications of various modes of inheritance of R‐genes for the ability of P. nemorum populations to colonize novel patches of B. vulgaris are discussed.