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.     

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.     

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.     

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.     

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。     

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.     

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.     

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.     

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.     

Population level correlation between pre-alighting and post-alighting host plant preference in the Glanville fritillary butterfly

1. In many populations of the Glanville fritillary butterfly Melitaea cinxia, ovipositing females exhibit a post‐alighting preference for one of the potential host plant species available. The work reported here aimed to establish whether females with different post‐alighting preferences can discriminate between their host plant species prior to alighting, and whether pre‐alighting and post‐alighting preferences are correlated at the population level. 2. Alighting and oviposition events were recorded for groups of females from six populations in greenhouse and field experiments. 3. Landing frequencies did not change with experience, indicating that M. cinxia females did not learn from previous encounters with host plants. 4. Females from populations exhibiting post‐alighting preference searched efficiently for their host plants in the sense that they landed mainly on the species on which they oviposited predominantly. Pre‐alighting and post‐alighting preferences were correlated at the population level. 5. The correlation between pre‐alighting and post‐alighting preferences helps to explain why in nature, where the host plants often occur in distinct patches, females are more likely to colonise habitat patches in which their preferred host plant is abundant.     

Egg laying by a butterfly on a fragmented host plant: a multi-level approach

Egg placement by herbivorous insects is an important step in their interaction with their host plants, and is the result of processes operating at different spatial and temporal scales. Although several studies have examined egg-placement patterns at different scales, this has rarely been achieved simultaneously using a multi-scale hierarchical approach. We studied egg placement in a rare European butterfly, Iolana iolas , whose larvae specifically feed on seeds of plants of the genus Colutea, using a hierarchical approach and Generalised Linear Mixed Modelling. The study was carried out in 2002 and 2003 in a ca 60 km² area in southern Madrid province, Spain, where the host plant, Colutea hispanica , has a highly fragmented distribution. We monitored in detail 132 plants in 24 patches and estimated the abundance of butterflies over the whole reproductive period of C. hispanica . We measured phenological, morphological and landscape variables potentially affecting egg-placement at three hierarchical levels: fruit, plant and host plant patch. Using egg presence–absence on mature fruits as the response variable, we found that eggs were more likely to be laid on fruits aged 1–2 weeks at the middle of the flowering period (fruit level), on large plants with a small number of shoots at the base (plant level), and in well connected host plant patches (patch level). Our results suggest that egg-placement is a process determined by factors operating at different levels: fruit, plant and host plant patch. Because egg-placement studies are often made with spatially correlated data, neglecting their intrinsic hierarchical nature could lead to equivocal conclusions.     

Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness

Invasive generalist ectoparasites provide a tool to study factors affecting expansion rates. An increase in the number of host species may facilitate geographic range expansion by increasing the number of suitable habitats and by affecting local extinction and colonization rates. A geographic perspective on parasite host specificity and its implications on range expansion are, however, insufficiently understood. We conducted a field study to explore if divergent host specificity could explain the observed variation in expansion rates between Fennoscandian populations of the deer ked (Lipoptena cervi), which is a blood-feeding ectoparasitic fly of cervids. We found that the rapidly expanding eastern population in Finland appears to specialize on moose, whereas the slowly expanding western population in Norway breeds successfully on both moose and roe deer. The eastern population was also found to utilize the wild forest reindeer as an auxiliary host, but this species is apparently of low value for L. cervi in terms of adult maintenance, reproductive output and offspring quality. Abundant numbers of roe deer and white-tailed deer were observed to be apparently uninfected in Finland, suggesting that host use is not a plastic response to host availability, but rather a consequence of population-level evolutionary changes. Locally compatible hosts were found to be the ones sharing a long history with the deer ked in the area. Cervids that sustained adult deer keds also allowed successful reproduction. Thus, host use is probably determined by the ability of the adult to exploit particular host species. We conclude that a wide host range alone does not account for the high expansion rate or wide geographic distribution of the deer ked, although loose ecological requirements would increase habitat availability.     

Life-history variation in relation to time constraints in a damselfly

Although variation within populations in plasticity to time constraints is expected with regard to hatching date, empirical studies are largely lacking. We studied life-history responses to time constraints manipulated by photoperiod and associated with hatching date in larvae of the damselfly Lestes viridis for two populations with a different hydroperiod. In a common garden experiment, early- and late-hatched larvae from both populations were reared at two photoperiods mimicking the start and the end of the egg-hatching season. In a reciprocal transplant experiment, early- and late-hatched larvae from both populations were reared in both ponds. In all these experiments, larvae were reared from egg hatching until adult emergence. Within both populations, larvae reared at the photoperiod indicating a late time point in the growing season, reduced development time to compensate for their perceived shorter development period. Growth rate, however, did not respond to photoperiod, resulting in a lower mass at emergence. As expected, both in the laboratory and in the field, larvae from eggs that hatched later in the season generally had a shorter development time and a faster growth rate, resulting in a higher mass at emergence compared to early-hatched larvae. This may explain the intriguing seasonal increase in mass at emergence in this species, and affect the predictions of optimality models. None of these life-history responses differed between the two populations, despite clear differences in time constraints linked to hydroperiod, suggesting the robustness of the observed patterns. Given the ubiquity of asynchronous hatching in nature, and the adaptive value of the observed differences between early- and late-hatched larvae, we expect the effects of hatching date on life-history plasticity to be widespread.     

Trade-offs underlying polyphagy in a facultative ant-tended florivorous butterfly: the role of host plant quality and enemy-free space

The underlying mechanisms mediating the use of multiple host plants were investigated in Parrhasius polibetes (Lycaenidae), a florivorous and facultative myrmecophilous butterfly. Plant traits such as presence of ant–treehopper associations as a source of enemy-free space, flower bud dimensions, toughness, thickness, trichomes, and the corresponding performance and wear of P. polibetes mandibles were examined for three natural hosts: Schefflera vinosa (Araliaceae), Pyrostegia venusta (Bignoniaceae) and Luehea grandiflora (Malvaceae). Parasitism levels of larvae found on the three hosts were also determined. Almost all Luehea had ant–treehopper associations, and all larvae found on this host were non-parasitized. Parasitism was low in larvae found on Schefflera, half of which hosted ant–treehopper associations. No ant–treehopper association was found on Pyrostegia, where parasitism was significantly higher compared to other hosts. In the laboratory, P. polibetes performed well on Schefflera, followed by Pyrostegia. No larvae survived when fed with Luehea. Flower buds of Luehea were thicker and tougher than those of Schefflera and Pyrostegia. Indeed, mandibles of larvae reared on Luehea showed substantial wear, whereas those reared either on Schefflera or Pyrostegia presented no significant damage. Additionally, we suggest that co-occurrence with ant–treehopper associations on a plant provides parasitoid-free space for P. polibetes larvae. Our results support the hypothesis that ecological trade-offs among host plants (i.e., food quality and enemy-free space) promote polyphagy in natural populations of P. polibetes. Host morphological traits seem to play a relevant role in P. polibetes performance. To our knowledge, this is the first report showing the costs of polyphagy in a myrmecophilous butterfly.     

Host plant utilization by butterfly larvae in the Andaman and Nicobar Islands (Indian Ocean)

The larval food plants of the butterflies of the Andaman and Nicobar islands have not been studied, although the butterfly fauna per se is fairly well known. For the first time we report the food plants of the larvae of 120 species of butterflies from these islands on the basis of laboratory rearing and field studies. This information is essential for the formulation of management programmes for butterfly conservation on these islands which are known to harbour critical swallowtail and (possibly) danaine faunas.