Host plant utilization in the comma butterfly: sources of variation and evolutionary implications

A major challenge in the study of insect-host plant interactions is to understand how the different aspects of offspring performance interact to produce a preference hierarchy in the ovipositing females. In this paper we investigate host plant preference of the polyphagous butterfly Polygonia c-album (Lepidoptera: Nymphalidae) and compare it with several aspects of the life history of its offspring (growth rate, development time, adult size, survival and female fecundity). Females and offspring were tested on four naturally used host plants (Urtica dioica, Ulmus glabra, Salix caprea, and Betula pubescens). There was substantial individual variation in host plant preference, including reversals in rank order, but the differences were largely confined to differences in the ranking of Urtica dioica and S. caprea. Different aspects of performance on these two plants gave conflicting and complementary results, implying a trade-off between short development time on U. dioica, and larger size and higher fecundity on S. caprea. As all performance components showed low individual variation the large variation in host plant preference was interpreted as due to alternative oviposition strategies on the basis of similar performance hierarchies. This indicates that the larval performance component of host-plant utilization may be more conservative to evolutionary change than the preference of ovipositing females. Possible macro-evolutionary implications of this are discussed.     

Genetics of host plant use and life history in the comma butterfly across Europe: varying modes of inheritance as a potential reproductive barrier

Comma butterflies (Nymphalidae: Polygonia c-album L.) from one Belgian site and three Spanish sites were crossed with butterflies from a Swedish population in order to investigate inheritance of female host plant choice, egg mass and larval growth rate. We found three different modes of inheritance for the three investigated traits. In line with earlier results from crosses between Swedish and English populations, the results regarding female oviposition preference (choice between Urtica dioica and Salix caprea) showed X-linked inheritance to be of importance for the variation between Sweden and the other sites. Egg mass and growth rate did not show any sex-linked inheritance. Egg mass differences between populations seem to be controlled mainly by additive autosomal genes, as hybrids showed intermediate values. The growth rates of both hybrid types following reciprocal crossings were similar to each other but consistently higher than for the two source populations, suggesting a nonadditive mode of inheritance which is not sex-linked. The different modes of inheritance for host plant preference vs. important life history traits are likely to result in hybrids with unfit combinations of traits. This type of potential reproductive barrier based on multiple ecologically important traits deserves more attention, as it should be a common situation for instance in the early stages of population divergence in host plant usage, facilitating ecological speciation.     

Geographical variation in insect developmental period: effect of host plant phenology on the life cycle of the bruchid seed feeder shape Kytorhinus sharpianus

The voltinism of the bruchid Kytorhinus sharpianus Bridwell (Coleoptera: Bruchidae) and the phenology of its host plant Sophora flavescens Aiton (Leguminosae) were observed at four latitudes: Aomori (40°46' N), Obanazawa (38°37' N), Kujiranami (37°21' N) and Mitsuma (36°05' N) in northeastern Honshu (Japan). Kytorhinus sharpianus life cycle ranged from bivoltine and partially trivoltine in the south to univoltine and partially bivoltine in the north. Sophora flavescens started growing later in spring at higher latitudes. However, the relative growth rate was higher in the north (Aomori) than in the south (Mitsuma). In parallel with this, the first-generation of adult K. sharpianus appeared later at higher latitudes. When the four local populations were reared at 24 °C, L16:D8 and 65% r.h., males developed faster than females. The mean developmental time showed a saw-toothed latitudinal cline. The reversion in the latitudinal trend of variation corresponded to the change in the major type of life cycles from univoltine to bivoltine. Two heat units throughout the year and post-fruiting period were calculated as the sums of degree-days above the developmental threshold (12 °C) of K. sharpianus. Both heat units decreased in parallel with each other with increasing latitude. The greater growth rate of hosts in the northern population compensated for the smaller heat units. In addition, when the heat units were divided by the degree-days needed to complete development, the numerical value was the approximate number of generations observed in each locality.     

Seasonal polyphenism and leaf mimicry in the comma butterfly

The comma butterfly, Polygonia c-album, exhibits seasonal polyphenism with a darkish winter morph and a lighter summer one. Phylogenetic analysis suggests that the winter morph represents the ancestral condition. We suggest two hypotheses for the evolution of the summer morph and the maintenance of seasonal polyphenism in the comma: (1) that the summer morph is better protected against predation on summer roost sites, whereas the winter morph is better protected on hibernation sites, and (2) that the summer morph is energetically less expensive and results from deallocation of resources from soma (e.g. dark wing pigmentation) to reproduction. We tested the antipredation hypothesis in experiments using great tits, Parus major, as predators on winter and summer morph commas presented simultaneously on tree trunks or on nettles. However, this hypothesis was not supported as the winter morph was better protected than the summer morph on both backgrounds. Predation when both morphs were present was lower on nettles, and summer morphs placed in exposed positions on tree trunks outdoors disappeared sooner than winter morphs placed on the same background. In addition, in a final experiment, 18 summer morphs released in their natural habitat in the evening exclusively chose leaves for roost sites, whereas 12 of 19 winter morphs chose a tree trunk, branch or twig. We conclude that evolution of the summer morph is consistent with the life history hypothesis and that its choice of summer roost sites is associated with a low predation pressure.     

Synchronization of gallers with host plant phenology

In addition to various bottom-up effects, the synchronization of herbivores with their host plant phenology determines quality and quantity of food resources and affects the preference–performance linkage and abundance of herbivores. The synchronization has a more critical meaning for such short-lived galling insects as cecidomyiid adults and young aphid stem mothers than for other insects. This review, first, presents general information about gall midges and gall aphids, together with their life history patterns and some ecological attributes. Second, some important topics of galling insect–host plant relation are briefly reviewed. Then, synchronization patterns between gall midge emergence and host plant phenology are analyzed to discuss the adaptive strategies of gall midges and to show how the amount of available food resources is affected by the time lag in synchronization. The spatial distribution pattern and the preference–performance linkage of aphid stem mothers is also discussed in relation to synchronization. Received: October 2, 1998 / Accepted: July 3, 2000     

菜粉蝶与其寄主植物金莲花

观察了用金莲花(TropaeolummajusL.)饲养的菜粉蝶PierisrapaeL.的发育情况,表明金莲花能使菜粉蝶完成世代发育,是其理想的寄主植物。国外有研究表明:将金莲花上取食的幼虫人为地转移到十字花科或其它寄主植物上,幼虫可正常取食,并最后发育为成虫;反之,将十字花科植物上取食的2龄至5龄的幼虫转移到金莲花上,则拒食外迁,最后全都饿死。然而,若将小麦胚芽人工饲料上饲养的幼虫转移到金莲花上,则幼虫正常取食。这是由于菜粉蝶幼虫在十字花科植物上取食的1龄阶段发展了对金莲花植株内所含的取食抑制化合物的敏感性,而在小麦胚芽人工饲料上取食的幼虫因一直接触取食抑制化合物而不对金莲花所含的取食抑制化合物产生敏感性之故。化学提取和昆虫行为实验证明,在金莲花中所含的取食抑制化合物的主要成分是绿原酸。     

Putting more eggs in the best basket: clutch-size regulation in the comma butterfly

Abstract.  1. Many studies have identified different factors influencing clutch-size regulation, primarily within various groups of insects. One prediction is that ovipositing females should increase clutch size with host quality. However, in many studies it is not clear whether ovipositing females are responding to host quality or quantity.
2. Females of the polyphagous comma butterfly, Polygonia c-album (L.), were allowed to oviposit on two hosts differing greatly in quality: the preferred host, stinging nettle ( Urtica dioica L.), and the low-ranked host, birch ( Betula pubescens Ehrh). Ovipositing females were observed visually and clutch sizes were recorded. The experiment was repeated in three different years; in total, 938 observations of oviposition events were made.
3. In all three years, females ovipositing on U. dioica laid larger clutches (median 1.6–1.85) compared with females ovipositing on B. pubescens (median 1.0–1.3) . The difference was significant in two out of three years and when all three years were pooled.
4. Thus, P. c-album females exhibit clutch-size regulation, with larger clutches on better hosts. It is suggested that the proximate mechanism is likely to be a response to the same stimuli used for female ranking of host plants in the preference hierarchy.     

The microbiome of the Melitaea cinxia butterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

Understanding of the ecological factors that shape intraspecific variation of insect microbiota in natural populations is relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe their gut microbiome and to identify potential ecological factors that determine its structure. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual and most likely the same genetic background. We observed that the caterpillars harboured microbial classes that varied among individuals and alternated between two distinct communities (one composed of mainly Enterobacteriaceae and another with more variable microbiota community). Even though the general structure of the microbiota was not attributed to the measured ecological factors, we found that phylogenetically similar microbiota showed corresponding responses to the sex and the parasitoid infection of the caterpillar and to those of the host plant's microbial and chemical composition. Our results indicate high among-individual variability in the microbiota of the M. cinxia caterpillar and contradict previous findings that the host plant is the major driver of the microbiota communities of insect herbivores.     

Estimating female reproductive success of a threatened butterfly: influence of emergence time and hostplant phenology

We estimated lifetime reproductive success of Euphydryas editha bayensis (Nymphalidae), a federally listed threatened butterfly, based on age-specific fecundity and both adult and offspring survival. Our results indicate that the relative timing of adult emergence and larval hosplant senescence strongly influenced reproductive success of females. For 1992, we estimated that only 8–21% of the eggs laid by females emerging on the 1st day of the 4-week flight season would produce larvae that reach diapause. This figure dropped to 1–5% for females emerging 7 days into the flight season. Within our entire sample, we estimated that 64–88% of the females produced offspring with less than a 2% probability of reaching diapause. These estimates are particularly striking given that they are based on only one source of larval mortality — prediapause starvation due to hostplant senescence. This dependence of reproductive success on the relative timing of female emergence and hostplant senescence may reduce effective population size and render E. editha bayensis especially vulnerable to local extinction events.     

Movement of the Apollo butterfly Parnassius apollo related to host plant and nectar plant patches

1. The movement of adults of the endangered Apollo butterfly, Parnassius apollo, was studied using mark–recapture data, within a population consisting of discrete patches of the species’ host plant (n = 43), which were segregated spatially from patches of the species’ main nectar plants (n = 14). 2. The Apollo routinely moved large distances (median 260 m, maximum 1840 m), and moved frequently between the two types of patches. Only 27% (28/105) of the recaptures were made on the same host plant patch as the release. 3. The population acts as a patchy population where the adults mix over the whole area, but successful reproduction can only take place in the discrete host plant patches. 4. Occurrence on a host plant patch was restricted by the area size of the host plant patch and the spatial configuration of nectar plant patches. Thus, although the Apollo is a good flyer, its movement over the patches is still constrained by the segregation of adult and larval resources.     

Genetics of diapause in the comma butterfly Polygonia c‐album

The processes of local adaptation and ecological speciation can be better understood by studying the genetic background of life‐history decisions. The sex chromosomes host genes for many population differences in the Lepidoptera and therefore the inheritance of diapause determination in the butterfly Polygonia c‐album may be hypothesized to be sex‐linked. In the present study, Polygonia c‐album (L.) from Spain and Sweden and hybrid offspring are raised under an LD 17 : 7 h photocycle that induces most pure Swedish individuals to develop into the diapausing dark morph and most pure Spanish individuals into the light and directly‐developing morph. If inheritance of the daylength threshold for diapause is X‐linked, as is known to be the case for host‐plant preferences, females should follow the developmental path of their male parents' populations. However, female hybrids instead have a diapause propensity intermediate to that of their parental stocks and, consequentially, diapause determination is not X‐linked. However, male hybrids eclose as the diapausing morph to a higher extent than females and, moreover, this pattern is more pronounced in the Spanish female × Swedish male cross than in the reciprocal cross. Hence, it is concluded that the genetic determination of the critical daylength for diapause is mainly autosomal but with some influence of sex‐linked genes and/or parental effects, possibly as an effect of the importance of protandry for males. Such sex effects could provide a starting point for the evolution of population differences inherited on the sex chromosomes.     

Geographical variation in host–ant specificity of the parasitic butterfly Maculinea alcon in Denmark

Abstract  1. Maculinea alcon uses three different species of Myrmica host ants along a north–south gradient in Europe. Based on this geographical variation in host ant use, Elmes et al . (1994) suggested that M. alcon might consist of three or more cryptic species or host races, each using a single and different host-ant species.
2. Population-specific differences in allozyme genotypes of M. alcon in Denmark ( Gadeberg & Boomsma, 1997 ) have suggested that genetically differentiated forms may occur in a gradient across Denmark, possibly in relation to the use of different host ants.
3. It was found that two host-ant species are indeed used as hosts in Denmark, but not in a clear-cut north–south gradient. Furthermore, specificity was not complete for many M. alcon populations. Of five populations investigated in detail, one used primarily M. rubra as a host, another exclusively used M. ruginodis , while the other three populations used both ant species. No population in Denmark used M. scabrinodis as a host, although this species was present in the habitat and is known to be a host in central and southern Europe.
4. In terms of number of parasites per nest and number of nests parasitised, M. rubra seems to be a more suitable host in populations where two host species are used simultaneously. Host-ant species has an influence on caterpillar size but this varies geographically. Analyses of pupae did not, however, show size differences between M. alcon raised in M. rubra and M. ruginodis nests.
5. The geographical mosaic of host specificity and demography of M. alcon in Denmark probably reflects the co-evolution of M. alcon with two alternative host species. This system therefore provides an interesting opportunity for studying details of the evolution of parasite specificity and the dynamics of host-race formation.     

Population structure in relation to host-plant ecology and Wolbachia infestation in the comma butterfly

Experimental work on Polygonia c‐album, a temperate polyphagous butterfly species, has shown that Swedish, Belgian, Norwegian and Estonian females are generalists with respect to host‐plant preference, whereas females from UK and Spain are specialized on Urticaceae. Female preference is known to have a strong genetic component. We test whether the specialist and generalist populations form respective genetic clusters using data from mitochondrial sequences and 10 microsatellite loci. Results do not support this hypothesis, suggesting that the specialist and generalist traits have evolved more than once independently. Mitochondrial DNA variation suggests a rapid expansion scenario, with a single widespread haplotype occurring in high frequency, whereas microsatellite data indicate strong differentiation of the Moroccan population. Based on a comparison of polymorphism in the mitochondrial data and sequences from a nuclear gene, we show that the diversity in the former is significantly less than that expected under neutral evolution. Furthermore, we found that almost all butterfly samples were infected with a single strain of Wolbachia, a maternally inherited bacterium. We reason that indirect selection on the mitochondrial genome mediated by a recent sweep of Wolbachia infection has depleted variability in the mitochondrial sequences. We also surmise that P. c‐album could have expanded out of a single glacial refugium and colonized Morocco recently.     

Advanced phenology of intraguild predators shifts herbivore host plant preference and performance

1. The abundance of insect herbivores is mediated by interactions with higher and lower trophic levels. This research asks (i) how phenological change across trophic levels affects host plant quality and selection for aphids, and (ii) what higher trophic level mechanisms drive aphid abundance. 2. Ligusticum porteri is a perennial host for the sap-feeding aphid Aphis asclepiadis and intraguild mirid predators (chiefly Lygus hesperus) in Colorado. We used long-term observational data to discover that aphids and mirids respond differently to phenological cues. These unique responses can impact aphid abundance through changes to host plant selection and quality. 3. We used behavioural choice assays to assess how advanced mirid phenology influences aphid host plant selection. More alates landed and reproduced on mirid-free control plants relative to host plants with prior mirid feeding. However, this preference did not correlate with aphid performance when we compared aphid relative growth rates between treatments. This suggests that advanced mirid phenology would impact aphid populations more through host plant choice, rather than reductions in host quality. The addition of mirids to experimental aphid colonies also demonstrated reduced aphid colony growth via predation. 4. We measured plant cues involved in host selection and found differences in volatile composition between plants with prior mirid feeding compared to control plants, providing the potential for aphids to detect enemy-free space using volatile cues.     

Inter and intraspecific variation on reproductive phenology of the Brazilian Atlantic forest Rubiaceae: ecology and phylogenetic constraints

The reproductive phenology of seven species of Rubiaceae from the Brazilian Atlantic rain forest was compared to evaluate the occurrence of phylogenetic constraints on flowering and fruiting phenologies. Since phenological patterns can be affected by phylogenetic constraints, we expected that reproductive phenology would be similar among plants within a family or genus, occurring during the same time (or season) of the year. Observations on flowering and fruiting phenology were carried out monthly, from December 1996 to January 1998, at Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba, S?o Paulo State, Brazil. Nine phenological variables were calculated to characterize, quantify and compare the reproductive phenology of the Rubiaceae species. The flowering patterns were different among the seven species studied, and the Kruskal-Wallis test indicated significant differences in flowering duration first flowering, peak flowering and flowering synchrony. The peaks and patterns of fruiting intensity were different among the Rubiaceae species studied and they differed significantly from conspecifics in the phenological variables fruiting duration, fruiting peak date, and fruiting synchrony (Kruskal-Wallis test). Therefore, we found no evidence supporting the phylogenetic hypotheses, and climate does not seem to constrain flowering and fruiting patterns of the Rubiaceae species in the understory of the Atlantic forest.     

Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology

Climatically driven Moran effects have often been invoked as the most likely cause of regionally synchronized outbreaks of insect herbivores without identifying the exact mechanism. However, the degree of match between host plant and larval phenology is crucial for the growth and survival of many spring-feeding pest insects, suggesting that a phenological match/mismatch-driven Moran effect may act as a synchronizing agent.We analyse the phase-dependent spatial dynamics of defoliation caused by cyclically outbreaking geometrid moths in northern boreal birch forest in Fennoscandia through the most recent massive outbreak (2000–2008). We use satellite-derived time series of the prevalence of moth defoliation and the onset of the growing season for the entire region to investigate the link between the patterns of defoliation and outbreak spread. In addition, we examine whether a phase-dependent coherence in the pattern of spatial synchrony exists between defoliation and onset of the growing season, in order to evaluate if the degree of matching phenology between the moth and their host plant could be the mechanism behind a Moran effect.The strength of regional spatial synchrony in defoliation and the pattern of defoliation spread were both highly phase-dependent. The incipient phase of the outbreak was characterized by high regional synchrony in defoliation and long spread distances, compared with the epidemic and crash phase. Defoliation spread was best described using a two-scale stratified spread model, suggesting that defoliation spread is governed by two processes operating at different spatial scale. The pattern of phase-dependent spatial synchrony was coherent in both defoliation and onset of the growing season. This suggests that the timing of spring phenology plays a role in the large-scale synchronization of birch forest moth outbreaks.     

Geographical variation in habitat choice and host suitability in the parasitoidAsobara rufescens

In the Netherlands, Asobara rufescens (Förster) (Hymenoptera: Braconidae) is a parasitoid of drosophilid larvae in decaying plant material. In several places in the Mediterranean, parasitoids looking very similar to A. rufescens were collected on fermenting substrates. A hybridization experiment showed that the parasitoids were indeed A. rufescens. In an olfactometer Portuguese A. rufescens do not have a preference for either the odour of yeast or decaying leaves, while their Dutch conspecifics prefer the odour of decaying leaves. The survival probability of Portuguese A. rufescens in Drosophila melanogaster Meigen (Diptera: Drosophilidae), a species typical for fermenting substrates, is much higher than the survival probability of Dutch A. rufescens in this host species. It is hypothesized that decaying plant material may be unsuitable for drosophilid larvae during part of the year in the Mediterranean, forcing A. rufescens there to broaden its microhabitat choice. The use of fermenting substrates brings A. rufescens in contact with its sibling A. tabida Nees, a species typical for fermenting substrates in most of Europe. Portuguese A. rufescens appear to be genetically isolated from A. tabida. In the Netherlands, where the two species occupy different microhabitats, there is only a premating barrier.