Genetic architecture for normal and novel host-plant use in two local populations of the herbivorous ladybird beetle, Epilachna pustulosa

Trade-offs in host-plant use are thought to promote the evolution of host specificity. However, usually either positive or no genetic correlations have been found. Whereas factors enhancing variation in overall viability have been claimed to mask negative genetic correlations, alternative hypotheses emphasize the sequential changes in genetic correlation in the course of host-range evolution. In this study, the genetic architectures of performances on different hosts were compared in two populations of the herbivorous ladybird beetle, Epilachna pustulosa, using three host plants, one being normal for both, one novel for only one population, and the other novel for both populations. The genetic correlations between larval periods on normal hosts were significantly positive whereas those between normal and novel hosts were not different from zero. There was no evidence for reduced genetic variation on the normal host-plants. These results suggest that the host-range is not restricted by the antagonistic genetic associations among exploitation abilities on different plant species, but rather that selection of different host-plants may improve the coordination between genes responsible for the use of different plants.     

Conspecific thistle plant selection by a herbivorous ladybird beetle, Epilachna pustulosa

Host selection by Epilachna pustulosa Kôno (Coleoptera: Coccinellidae) was surveyed in an area of about 130 ares, focusing on the role of the spatial distribution pattern of the host plant, thistle Cirsium kamtschaticum Ledeb. (Asteraceae) and the environmental conditions of habitats where thistle plants were growing. A total of 198 thistle clones were found in the area studied, and approximately 40% showed some degree of E. pustulosa infestation by July. Eggs were only oviposited on thistle clones that were fed on by adults. Adult beetles and egg masses of E. pustulosa showed an aggregated distribution in the earlier season (June) among thistle clones. The distribution of adults became more random (but still aggregated) by the later season (July), along with an increase in the number of infested clones. Multiple logistic regression analyses revealed that clone size and soil moisture were consistently important for the beetle's choice of clones to feed on. The other logistic regression analyses indicated that thistle‐clone size and sunlight condition influenced egg distribution. Thistle clone selection by E. pustulosa changed with season from a rather strict selection in June to a more obscure one in July, expanding the range of thistle clones used as feeding and oviposition substrate.     

Consequences of adult size for survival and reproductive performance in a herbivorous ladybird beetle

Abstract.

• 1 A univoltine herbivorous ladybird beetle Epilachna niponica (Coleoptera: Coccinellidae) shows a large variation in adult size within a population.
• 2 Large adults had higher survival from emergence to the reproductive season, and the size-dependent adult survival was most apparent during hibernation. On the other hand, adult survival during pre-hibernation contributed little to size-dependent overall survival.
• 3 Neither reproductive lifespan nor lifetime fecundity were a function of adult size, though large females produced larger size of egg batches.
• 4 Size of adult beetles was significantly reduced by leaf damage to plants on which they grew up on larval stage. Since leaf herbivory increases through the season, late emerged adults that were subjected to food deterioration during the larval period were smaller than early-emerged individuals.

     

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.     

Variable correspondence of female host preference and larval performance in a phytophagous ladybird beetle Epilachna pustulosa (Coleoptera: Coccinellidae)

Genetic and environmental factors causing intraspecific variation of the thistle Cirsium kamtschaticum Ledeb. as a host plant of the phytophagous ladybird Epilachna pustulosa Kôno were investigated through simple food-choice tests and rearing of larvae. Two thistle clones (T1U₁ and T4H₂) were used, originally growing approximately 12 km apart. A previous study showed that adult female ladybirds preferred T1U₁ to T4H₂, and that larval performance was better on T1U₁, when leaves from the clones in situ were examined. The two clones retained their characteristics with respect to beetle preference after transplantation into a common garden. However, the difference between T1U₁ and T4H₂ with respect to larval performance was reduced after the transplantation. When leaves from shoots of T1U₁ exposed to different sunlight intensities were offered, adult female ladybirds did not show obvious preferences. Larval eclosion rates increased significantly with the increase in leaf sunlight intensity exposure. These results suggest strongly that both genetic and environmental factors are involved in interclonal variation of thistle quality in beetle preference and/or performance. It is suggested that the quality of thistle leaves for larval performance is largely affected by environmental factors, while leaf quality for beetle preference may be determined strictly by genetic factors. Under certain conditions, E. pustulosa females may behave maladaptively, preferring plants not appropriate for larval growth, or not choosing plants appropriate for the larval growth.     

Host plant suitability of a recently naturalized thistle Cirsium vulgare (Asteraceae) for a phytophagous ladybird beetle,Epilachna pustulosa (Coleoptera: Coccinellidae)

The phytophagous ladybird beetle, Epilachna pustulosa Kôno occurs mainly on the thistle Cirsium kamtschaticum Ledeb. In recent years, we have confirmed feeding and oviposition by E.pustulosa, and some degree of larval development of this beetle, on a naturalized congeneric thistle, Cirsium vulgare (Savi) Tenore. In this study, we assessed the host suitability of C.vulgare for E.pustulosa, using larval rearing and simple food choice tests, by comparing the performance on, and preference for, their legitimate host C.kamtschaticum. All experiments were initiated in July, when the utilization of C.vulgare by E.pustulosa became obvious. For larval performance, E.pustulosa showed a lower eclosion rate, shorter developmental duration and smaller body size when reared on C.vulgare than on C.kamtschaticum. Cirsium vulgare appeared to be a less adequate larval food than C.kamtschaticum. Adult feeding preference was altered seasonally; females preferred C.kamtschaticum to C.vulgare in a food choice test conducted in early July, whereas they showed the opposite preference in tests conducted in mid and late July. The utilization of C.vulgare by E.pustulosa appeared to be induced by qualitative deterioration of C.kamtschaticum leaves in July, which resulted in increased dispersion of adult beetles.     

Adaptive change and conservatism in host specificity in two local populations of the thistle-feeding ladybird beetle Epilachna niponica

We investigated geographic differences in the host specificity of Epilachna niponica Lewis (Coleoptera: Coccinellidae). The Yuwaku population feeds mainly on Cirsium matsumurae Nakai (Asteraceae) and secondarily on Cirsrium kagamontanum Nakai. The Asiu population, located 150 km away from the Yuwaku, feeds exclusively on C. ashiuense Yokoyama et T. Shimizu. Under laboratory conditions, we examined the differences between the two populations in adult feeding acceptance, adult feeding preference, and larval performance, using several closely related thistle species and varieties, including their native hosts. In the Asiu population, adult beetles clearly avoided the host of the Yuwaku population, C. kagamontanum, and no larvae were able to complete their development, whereas in the Yuwaku population, adults accepted and even preferred it to some other thistle species, and about 10% of first instar larvae became adults. This indicates that the Yuwaku population evolved its feeding preference and physiological adaptation to C. kagamontanum through a utilization of this low‐ranked host under natural conditions. Apart from C. kagamontanum, the two populations showed a similar host susceptibility pattern, indicating that this ladybird beetle has a conserved hierarchy in feeding preference and growth performance. We also observed adult leaf choice behavior when given different thistle species, and found that difference in biting rate after palpation determined the leaf areas consumed, implying that factors on the leaf surface played an important role in the choice.     

Genetic variation in larval period and pupal mass in an aphidophagous ladybird beetle (Harmonia axyridis) reared in different environments

Abstract Genetic trade‐offs for host plant use are hypothesized to facilitate the diversification of insect populations through specialization to their host plants. Previous studies mainly estimated the architecture of genetic variances and covariances in herbivorous species with discrete and limited types of host species. In contrast to herbivores, the relative abundance of resources for predatory species fluctuates in time and space, causing a more unpredictable encounter with prey species. The ecological characteristics of resource use might result in a differential mode of selection for herbivorous and predatory species, which could be reflected in a differential genetic architecture of developmental traits such as the duration of larval stage (henceforth referred to as larval period) and size of pupa (measured as pupal weight). This paper presents results from a study on the genetic architecture of larval period and pupal mass of an aphidophagous ladybird beetle, Harmonia axyridis Pallas, in different resource environments. Beetles reared on Acyrthosiphon pisum (Harris) showed a shorter developmental period and a heavier pupal mass than their siblings on Aphis craccivora Koch or on artificial diet, while the average larval period and pupal mass on A. craccivora and the artificial diet were similar. Further analyses of the genetic architecture suggest that the developmental traits on the two aphid species are genetically correlated, while there are only weak or no genetic correlations between these two traits on the two aphid preys and the artificial diet. Thus, the results suggest that the patterns of genotypic relationships between developmental traits differ from the phenotypic ones. The effects of past selection on the genetic architecture and the possible cause of the genetic correlation are discussed, as well as consequences for mass rearing for biological control.     

Genetic basis and fitness consequences of winglessness in the two-spot ladybird beetle, Adalia bipunctata

The genetic basis and fitness consequences of winglessness were investigated in the two-spot ladybird beetle, Adalia bipunctata. By breeding lines from a wingless individual found at The Uithof, Utrecht in The Netherlands, the wingless condition was confirmed to be under the control of a major allele, recessive to the wild type. Wingless individuals, on average, had a longer developmental period, a lower egg production and a shorter lifespan than the wild type with wings, suggesting that the expression of the wingless allele has functionally interrelated gene actions involving a wide range of fitness components. While the wingless allele influences various traits, significant among-family variation in the degree of winglessness suggests that its phenotypic expression is also dependent on the genetic background and modifier loci. Furthermore, there was a consistent pattern of correlation between the degree of winglessness and life history traits; the most extreme wingless individuals showed the lowest fitness while those with more fully developed wings tended to have the highest fitness. This correlation suggests that the modifier genes influence both wing formation and fitness components. The significance of such epistatic effects to the evolution of flightlessness in insects is discussed.     

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.     

Heterospecific sperm reduction in interspecific crosses between two closely related phytophagous ladybird beetles,Henosepilachna vigintioctomaculata and H. pustulosa (Coleoptera: Coccinellidae)

In interspecific crosses, a mismatch in internal physiological conditions between two species can reduce sperm viability in the interval from insemination to fertilization, leading to gametic isolation. Two closely related Japanese phytophagous ladybird beetles, Henosepilachna vigintioctomaculata and H. pustulosa, show several isolating barriers, including reduction in the number of heterospecific sperm in the female reproductive tract and low egg‐hatching rates in interspecific matings. However, the mechanisms of these two potential isolating barriers and the association between them are unknown. Here we investigated temporal changes in the number of sperm stored in the female reproductive tract and egg‐hatching rates in inter‐ and intraspecific crosses between these species. Although the number of sperm decreased after both inter‐ and intraspecific crosses, the reduction was more drastic in inter‐ than in intraspecific crosses for females of both species. Most of the sperm reduction occurred early on, during sperm transfer from the bursa copulatrix to the paired ampullae of the common oviduct (the sperm storage organs). These two species also demonstrated stably low egg‐hatching rates in interspecific crosses. Since the degree and timing of the sperm reduction did not correlate with egg‐hatching rates, the reduction in heterospecific sperm in interspecific crosses may not directly cause the low hatching rates. These two isolating barriers could be different expressions of the physiological mismatch and/or genetic incompatibility between gametes of these species.     

Adaptation to a new host plant, Centrosema pubescens (Fabales: Leguminosae), by the phytophagous ladybird beetle, Epilachna vigintioctopunctata (Coleoptera: Coccinellidae), in tropical Asia

The host suitability of Centrosema pubescens (Leguminosae) was evaluated within two sympatric populations feeding on Solanum plants (Solanaceae) and C. pubescens in Epilachna vigintioctopunctata in Malaysia (Kuala Lumpur) and Indonesia (Bogor and Padang). In the Bogor and Padang populations, Centrosema strains had a significantly higher emergence rate than sympatric Solanum strains. In Kuala Lumpur, there was no significant difference in emergence rates between the two strains. When Centrosema strains from Kuala Lumpur and Padang were reared and maintained solely on Solanum plants, the emergence rate on C. pubescens gradually decreased with successive rearing generation and resulted in 0% in the 7th or 20th generations. These findings suggest that the current host suitability of C. pubescens depends on the previous experience of each population with the use of this plant as a host. However, we were not able to demonstrate from laboratory selection that Solanum strains increase the host adaptation to C. pubescens because every Solanum strain became extinct in the third generation when reared solely on C. pubescens. Received: August 16, 1999 / Accepted: June 5, 2000     

Sex ratios and genetic variation in a functionally androdioecious species,Schizopepon bryoniaefolius (Cucurbitaceae)

Androdioecy, coexistence of hermaphrodites and males, is an extremely rare breeding system in angiosperms. In the present study, Schizopepon bryoniaefolius (Cucurbitaceae) was confirmed to be functionally androdioecious based on observations of floral and pollen morphology and bagging experiments. Six out of the 11 studied populations consisted of only hermaphrodites, while the other five populations were androdioecious and the frequencies of males were consistently lower than those of hermaphrodites (5.5–28.3%). To understand the consequences of an androdioecious breeding system, genetic variation was estimated using four polymorphic allozyme loci. The degree of genetic differentiation among 11 populations was high (G_ST = 0.688). Inbreeding coefficients (F_IS) for all loci significantly deviated from zero. In particular, the F_IS values averaged across the polymorphic loci in hermaphrodite populations were close to unity, suggesting that hermaphrodites are predominantly selfing in the absence of males. A significant negative correlation was found between the frequencies of males and inbreeding coefficients, indicating that outcrossing rates depend on the population sex ratio.     

Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F(1) hybrid inviability, and sexual selection against F(1) hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.     

Polymorphism in a flea beetle for the ability to use an atypical host plant

The flea beetle Phyllotreta nemorum L. (Coleoptera: Chrysomelidae: Alticinae) is polymorphic for its ability to use Barbarea vulgaris R. Br. (Brassicaceae) as a host plant. The genetic factors influencing this ability show both sex-linked and autosomal inheritance. Evidence was found for the presence of major genes such as those found in earlier studies, but also of genes with a smaller effect which have not previously been found. Although the ability to survive on B. vulgaris exists in most populations in eastern Denmark, it is usually at a low frequency. Beetles collected on B. vulgaris, however, usually produced larvae that survived on this plant. The inheritance and the abundance of the ability to use B. vulgaris are discussed in the context of the evolution of the interaction between P. nemorum and its atypical host plant.     

Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant

Abstract 1. The herbaceous plant Solanum carolinense (L.) (Solanaceae) is host to a number of specialist insects, including the leaf-feeding beetles Epitrix fuscula (Crotch) and Leptinotarsa juncta (Germar) (Coleoptera: Chrysomelidae). Potted individuals of S. carolinense were subjected to one of two treatments: exposure to herbivory by E. fuscula or exclusion of all herbivores. The effects of E. fuscula herbivory on larval performance and oviposition preference of L. juncta were investigated.
2. Although the masses of the L. juncta pupae did not differ between the two treatments, larvae feeding on damaged plants developed more slowly than those feeding on undamaged plants.
3. In both paired leaf choice trials and whole plant choice trials, larvae of L. juncta showed no preference for undamaged versus damaged hosts.
4. In a field transplant experiment, adult L. juncta females showed slight feeding preferences and strong oviposition preferences for undamaged plants versus plants that had been fed on by E. fuscula .
5. The results are discussed with reference to their implications for plant-mediated competition among herbivores and constraints on the evolution of plant resistance.     

Life history traits of pest and non-pest populations in the phytophagous ladybird beetle,Epilachna niponica (coleoptera, coccinellidae)

Life history traits of the phytophagous ladybird beetle,Epilachna niponica were compared between a non-pest population feeding on wild thistle and a pest population feeding on cultivated solanaceous crops, mainly potato. The pest population had larger females, a higher population growth rate, a more continuous oviposition schedule, and a shorter developmental period in the immature stages, compared with the non-pest population. The two populations showed no clear differences in phenology from spring to autumn, egg mass size, hatchability, and larval survival rate. Significant differences were found in number of eggs laid per female during the first and second periods, and in the developmental period of the immature stages. These life history traits were influenced primarily by food plant. A higher fecundity and shorter immature period appear to be readily altered by the host shift from thistle to potato.     

Genetic architecture of sexual dimorphism in a subdioecious plant with a proto-sex chromosome

The rise of sexual dimorphism is thought to coincide with the evolution of sex chromosomes. Yet because sex chromosomes in many species are ancient, we lack empirical evidence of the earliest stages of this transition. We use QTL analysis to examine the genetic architecture of sexual dimorphism in subdioecious octoploid Fragaria virginiana. We demonstrate that the region housing the male-function locus controls the majority of quantitative variation in proportion fruit set, confirming the existence of a proto-sex chromosome, and houses major QTL for eight additional sexually dimorphic traits, consistent with theory and data from animals and plants with more advanced sex chromosomes. We also detected autosomal QTL, demonstrating contributions to phenotypic variation in sexually dimorphic traits outside the sex-determining region. Moreover, for proportion seed set we found significant epistatic interactions between autosomal QTL and the male-function locus, indicating sex-limited QTL. We identified linked QTL reflecting trade-offs between male and female traits expected from theory and positive integration of male traits. These findings indicate the potential for the evolution of greater sexual dimorphism. Involvement of linkage groups homeologous to the proto-sex chromosome in these correlations reflects the polyploid origin of F. virginiana and raises the possibility that chromosomes in this homeologous group were predisposed to become the sex chromosome.