Seasonal selection and resource dynamics in a seasonally polyphenic butterfly

Seasonal polyphenisms are widespread in nature, yet the selective pressures responsible for their evolution remain poorly understood. Previous work has largely focussed either on the developmental regulation of seasonal polyphenisms or putative ‘top‐down’ selective pressures such as predation that may have acted to drive phenotypic divergence. Much less is known about the influence of seasonal variation in resource availability or seasonal selection on optimal resource allocation. We studied seasonal variation in resource availability, uptake and allocation in Araschnia levana L., a butterfly species that exhibits a striking seasonal colour polyphenism consisting of predominantly orange ‘spring form’ adults and black‐and‐white ‘summer form’ adults. ‘Spring form’ individuals develop as larvae in the late summer, enter a pupal diapause in the fall and emerge in the spring, whereas ‘summer form’ individuals develop directly during the summer months. We find evidence for seasonal declines in host plant quality, and we identify similar reductions in resource uptake in late summer, ‘spring form’ larvae. Further, we report shifts in the body composition of diapausing ‘spring form’ pupae consistent with a physiological cost to overwintering. However, these differences do not translate into detectable differences in adult body composition. Instead, we find minor seasonal differences in adult body composition consistent with augmented flight capacity in ‘summer form’ adults. In comparison, we find much stronger signatures of sex‐specific selection on patterns of resource uptake and allocation. Our results indicate that resource dynamics in A. levana are shaped by seasonal fluctuations in host plant nutrition, climatic conditions and intraspecific interactions.     

Sexual selection constrained by life history in a butterfly

Trait evolution via sexual selection has traditionally been viewed as isolated from life-history constraints. Recent theoretical treatments, however, predict that costly sexually selected characters should be mediated by the same allocational trade-offs that apply to more conventional aspects of reproductive investment. Participation in risky competitive behaviours, for example male-male combat, should therefore increase as the opportunity for future reproduction declines. However, the demonstration of such trade-offs has proven to be elusive due to concomitant age-based variation in the physical determinants of fighting 'ability'. Here, I exploit the unique nature of a butterfly contest system to provide compelling evidence for lifetime partitioning of risky and aggressive sexually selected behaviours. I show that male Hypolimnas bolina become more willing to persist in contests over mating territories, and more generally accepting of injury risks, as they age. Contest persistence in this species is not mediated simply by physical condition, and I experimentally isolate the effect of ageing per se from resource ownership and previous contest experience. These results demonstrate how sexually selected behaviours can be ultimately mediated by a shifting trade-off between contemporary reproductive effort and future opportunities.     

Microhabitat selection in a grassland butterfly: a trade-off between microclimate and food availability

Understanding the factors that determine habitat quality is vital to ensuring appropriate habitat management. The main objective of this study was to assess the microhabitat preferences of egg-depositing females of the Grizzled Skipper (Pyrgus malvae) in calcareous grasslands of the Diemel Valley (Central Germany) for defining habitat quality. Based on this knowledge, we make management recommendations for the conservation of this threatened species. P. malvae generally preferred open and warm oviposition sites. However, there were considerable differences in the environmental conditions, depending on the selected host plant. On the small Potentilla tabernaemontani plants that grew in sparse vegetation with low-growing turf, mostly only one egg was found per plant. In contrast, occupied Agrimonia eupatoria host plants were larger and more prominent, regularly having more than one egg, and grew at sites with a taller and denser vegetation. The observed oviposition pattern reflects a trade-off between microclimate and food availability: Usually, occupied P. tabernaemontani plants grow under favourable microclimatic conditions. However, during hot years the risk of desiccation is high, leading to food shortage. In contrast, A. eupatoria generally provides more biomass, thrives on deeper soils and the vegetation has a cooler microclimate: hence, food shortage is somewhat unlikely. To meet the described habitat requirements of P. malvae, traditional rough grazing by sheep and goats seemed to be the most appropriate land management strategy. The re-introduction of coppicing in woodlands, particularly adjacent to calcareous grasslands, would also be beneficial.     

Antagonistic, stage-specific selection on defensive chemical sequestration in a toxic butterfly

Larvae of the pipevine swallowtail ( Battus philenor ) sequester toxic alkaloids called aristolochic acids from their Aristolochia host plants, rendering both larvae and adults chemically defended against most predators. Using a chemically controlled artificial diet, we observed substantial among-family variation in sequestration ability and larval developmental rate in a population occurring in central Texas. Early instar larvae from families that sequester greater amounts of aristolochic acid showed increased survivorship in a field experiment in which cohorts from each family were exposed to natural predators, whereas among-family variation in growth rate did not predict survivorship. Conversely, the aristolochic acid content of adult butterflies was negatively correlated with adult fat content, a fitness correlate. Sequestration ability positively affects the probability of larval survivorship, but at the cost of adult fat content. The costs and benefits of aristolochic acid sequestration vary during the course of the butterfly's development, and these antagonistic selection pressures may explain why variation in sequestration ability persists in wild populations.     

Accommodating natural and sexual selection in butterfly wing pattern evolution

Visual patterns in animals may serve different functions, such as attracting mates and deceiving predators. If a signal is used for multiple functions, the opportunity arises for conflict among the different functions, preventing optimization for any one visual signal. Here we investigate the hypothesis that spatial separation of different visual signal functions has occurred in Bicyclus butterflies. Using phylogenetic reconstructions of character evolution and comparisons of evolutionary rates, we found dorsal surface characters to evolve at higher rates than ventral characters. Dorsal characters also displayed sex-based differences in evolutionary rates more often than did ventral characters. Thus, dorsal characters corresponded to our predictions of mate signalling while ventral characters appear to play an important role in predator avoidance. Forewing characters also fit a model of mate signalling, and displayed higher rates of evolution than hindwing characters. Our results, as well as the behavioural and developmental data from previous studies of Bicyclus species, support the hypothesis that spatial separation of visual signal functions has occurred in Bicyclus butterflies. This study is the first to demonstrate, in a phylogenetic framework, that spatial separation of signals used for mate signalling and those used for predator avoidance is a viable strategy to accommodate multiple signal functions. This signalling strategy has important ramifications on the developmental evolution of wing pattern elements and diversification of butterfly species.     

Variation in utilization of young leaves by a swallowtail butterfly across a deer density gradient

Phytophagous insects can be affected by plant trait-mediated indirect effects of large herbivores, but little is known regarding how these effects change in response to different densities of large herbivores. To assess the response of an insect to plant qualitative change, the response of a woody vine (Aristolochia kaempferi) to browsing by sika deer (Cervus nippon) and utilization of young leaves by a swallowtail butterfly (Byasa alcinous) were investigated across a deer density gradient. Natural and simulated deer browsing stimulated the regrowth of A. kaempferi and improved nutritional and physical quality of leaves. Young leaves were frequently observed in areas with high deer densities. The proportion of young leaves among the leaves selected for oviposition was higher than their proportion of the total number of leaves. In areas with low deer densities, the utilization of young leaves by B. alcinous increased linearly with deer density, whereas in areas with high deer densities, the utilization of young leaves was around 90%.     

Realized correlated responses to artificial selection on pre-adult life-history traits in a butterfly

We use artificial selection experiments targeted on egg size, development time or pupal mass within a single butterfly population followed by a common-garden experiment to explore the interactions among these life-history traits. Relationships were predicted to be negative between egg size and development time, but to be positive between development time and body size and between egg size and body size. Correlated responses to selection were in part inconsistent with these predictions. Although there was evidence for a positive genetic correlation between egg and body size, there was no support for genetic correlations between larval development time and either egg size or pupal mass. Phenotypic correlations among the three target traits of selection gave comparable results for the relationships between egg mass and development time (no association) as well as between egg mass and pupal mass (positive association), but not for the relation between development time and pupal mass (negative phenotypic correlation). In summary, correlated responses to selection as well as phenotypic correlations were rather unpredictable. The impact of variation in acquisition and allocation of energy as well as of the benign conditions used deserve further investigation.     

Food selection by brook trout in a subalpine stream

The diet and food selection of brook trout (Salvelinus fontinalis) and macroinvertebrate drift are described for a high altitude stream (3 205 m above mean sea level) adjacent to the alpine zone on the Snowy Range in the Medicine Bow National Forest, Wyoming. Diet composition differed between brook trout of two length classes, 150 mm and > 150 mm in total length. The number of prey organisms per stomach generally declined and the proportion of terrestrial prey items increased from July to September, 1985. Fish of both length classes selected for Trichoptera and Coleoptera over the three sampling months, and fish > 150 mm also selected for terrestrial insects in August and September.The Unit is jointly supported by the University of Wyoming, the Wyoming Game and Fish Department, and the US Fish and Wildlife ServiceThe Unit is jointly supported by the University of Wyoming, the Wyoming Game and Fish Department, and the US Fish and Wildlife Service     

On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection

Many organisms display phenotypic plasticity as adaptation to seasonal environmental fluctuations. Often, such seasonal responses entails plasticity of a whole suite of morphological and life‐history traits that together contribute to the adaptive phenotypes in the alternative environments. While phenotypic plasticity in general is a well‐studied phenomenon, little is known about the evolutionary fate of plastic responses if natural selection on plasticity is relaxed. Here, we study whether the presumed ancestral seasonal plasticity of the rainforest butterfly Bicyclus sanaos (Fabricius, 1793) is still retained despite the fact that this species inhabits an environmentally stable habitat. Being exposed to an atypical range of temperatures in the laboratory revealed hidden reaction norms for several traits, including wing pattern. In contrast, reproductive body allocation has lost the plastic response. In the savannah butterfly, B. anynana (Butler, 1879), these traits show strong developmental plasticity as an adaptation to the contrasting environments of its seasonal habitat and they are coordinated via a common developmental hormonal system. Our results for B. sanaos indicate that such integration of plastic traits – as a result of past selection on expressing a coordinated environmental response – can be broken when the optimal reaction norms for those traits diverge in a new environment.     

Correlated responses to selection on female egg size in male reproductive traits in a butterfly

Genetic correlations between male and female traits can act as evolutionary constraints and, if involving reproductive traits, potentially influence sexual selection. Artificial selection on egg size in the tropical butterfly Bicyclus anynana has yielded highly divergent lines. Here we report evidence for correlated evolution in male traits. Males from the large-egg selected lines produced significantly heavier spermatophores independent of body size and tended to have more fertile sperm stored in their reproductive tracts than those from the small-egg selected lines. This may be due to an underlying genetic correlation in reproductive effort between the sexes. However, non-fertile sperm number and testis size remained unaffected by selection on egg size. Phenotypic correlations within an unselected population revealed that spermatophore mass and fertile sperm number, but not testis size and non-fertile sperm number, were positively related to male body size, and that larger spermatophores contained more fertile, but not non-fertile sperm. In addition, males provided larger females with bigger spermatophores and more fertile sperm, indicating males may be exercising mate choice during copulation.     

Food selection by beavers

Summary Multidimensional contingency tables provide a powerful new statistical tool for analyzing interactions among several variables in an ecological study. This technique is applied to a study of selectivity in tree-cutting by two colonies of beavers in central Massachusetts.At the Blue Heron Cove colony, selection depends jointly on genus and diamter. Beavers cut birch of all diameters available but avoid large diameter maples, pines, and oaks. These beavers are choosy generalists: they show clear preferences in cutting various genera of trees for food yet they cut substantial numbers of trees of non-preferred genera. At the Tamplin Road Pond colony, discrete sites of concentrated cutting activity differ in genera and diameters of trees selected. Trees of all diameters are cut at one site close to water, small diameter trees are selected at two other sites farther from water. Ironwood is preferred at one site but selected against at two other sites. This difference between sites in generic selectivity has two plausible explanations: (1) tree species differ in nutritional and other chemical value between sites, (2) beavers sample trees of the various species present at some sites in order to assess the value of such sites as foraging areas.     

Plant ploidy level influences selection by butterfly seed predators

Polyploidization is a common route to plant diversification. Polyploids often differ from their progenitors in size, flower number, flower size and flowering phenology. Such differences may translate into differences in the intensity of interactions with animals. Here we investigated the impact of the ploidy-related differences in tetraploids and octoploids of the perennial herb Cardamine pratensis on pre-dispersal seed predation by the butterfly Anthocharis cardamines . The probability of escaping attack was lower for octoploids than for tetraploids, even after accounting for the fact that octoploids were larger and had fewer flowers than tetraploids. Flower shoot size was correlated with probability of attack in tetraploids but not in octoploids. Differences in plant traits associated with polyploidization can alter interactions with animals, and animal-mediated differences in trait selection between ploidy types can contribute to their further divergence.     

Food selection of Coregonus lavaretus in a brackish water ecosystem

This study examined how variability in the abundance and biomass structure of benthic invertebrates affected the feeding choice of the whitefish Coregonus lavaretus on a hard bottom habitat of the brackish Baltic Sea. In general, crustaceans such as Idotea balthica and Gammarus spp. were preferred over molluscs. Although being the most numerous taxon in the invertebrate samples, Mytilus trossulus was the lowest ranking in C. lavaretus food preference. The availability of benthic invertebrate prey set the dietary range of fish but the selectivity largely described fish feeding within this range. There was no clear link between fish predation and the dominance structure of benthic invertebrate communities, suggesting that species composition, abundance and biomass of invertebrate species had no impact on the feeding selectivity of the fish. Thus, while fish predation may not affect the dominant species within a benthic community, due to strong selectivity fish may impose strong pressure on some rarer but highly preferred invertebrate prey species.     

Towards a theory of the evolution of butterfly colour patterns under directional and disruptive selection

Two general models for the transspecific evolution of butterfly colour patterns are advanced: directional selection acting equally on both sexes, and disruptive selection involving periods of polymorphism. To consider possible outcomes of me latter process, a morphism notation based on an integrated classification for polymorphism and sexual dimorphism is developed. This notation is used to examine the properties of all morphism transformations possible from the minimal expressions of the nine morphism categories, as reached through defined minimum step changes. The significance of such pathway models is analysed in terms of general properties of butterfly polymorphism. The potential use of pathway models in evolutionary studies is briefly discussed, mainly with respect to phylogenetics, and ideas on the evolution of genetic dominance.     

Simultaneous selection on two fitness-related traits in the butterfly Bicyclus anynana

Abstract. Theory about the role of constraints in evolution is abundant, but few empirical data exist to describe the consequences a bias in phenotypic variation has for micro evolution. Responses to natural selection can be severely hampered by a genetic correlation among a suite of traits. Constraints can be studied using antagonistic selection experiments, that is, two-trait selection in opposition to this correlation. The two traits studied here were development time and wing pattern (eyespot size) in the butterfly Bicyclus anynana , both of which have a clear adaptive significance. Rates of response were higher for eyespot size than for development time, but were independent of the concurrent selection (either in the same direction as the correlation or perpendicular to it). Regimes differed in both traits in all directions after 11 generations of selection. The uncoupling lines had higher relative responses than the synergistic lines in development time and equal relative responses in eyespot size. The patterns for eyespot size (reaction norms) were consistent across different rearing temperatures. Differences in lines selected for fast and slow development time were more pronounced at lower temperatures, irrespective of the direction of joint wing pattern selection. Furthermore, correlated responses in pupal weight and growth rate were observed; lines selected for a slower development had higher pupal weights, especially at lower temperatures. The response of the uncoupling lines was not hampered by a lack of selectable genetic variation, and the relative response in the development time was larger than expected based on response in the coupled direction and quantitative genetic predictions. This suggests that the structure of the genetic architecture does not constrain the short-term, independent evolution of both wing pattern and development time.     

Food supply and prey selection in planktivorous cyprinidae

Summary In small Bavarian lakes, the gut contents of the Cyprinid fish roach (Rutilus rutilus), rudd (Scardinius erythrophtalamus), bream (Abramis brama) and bleak (Alburnus alburnus), and the actural food supply during the fish's feeding period were examined in relation to the species composition of zooplankton. Accompanied by feeding experiments in the laboratory, the selective effect of fish predation could be attributed to the distribution patterns of prey and predator in time and space, to the prey's specific visibility and escape ability and, to some extent, to the fish's active choice. The possibility that the species composition of zooplankton is regulated was indicated only in the fish's positively abundance-dependent preference for the prey types and restricted to only a few plankter species.     

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.     

The evolution of alternative developmental pathways: footprints of selection on life-history traits in a butterfly

Developmental pathways may evolve to optimize alternative phenotypes across environments. However, the maintenance of such adaptive plasticity under relaxed selection has received little study. We compare the expression of life-history traits across two developmental pathways in two populations of the butterfly Pararge aegeria where both populations express a diapause pathway but one never expresses direct development in nature. In the population with ongoing selection on both pathways, the difference between pathways in development time and growth rate was larger, whereas the difference in body size was smaller compared with the population experiencing relaxed selection on one pathway. This indicates that relaxed selection on the direct pathway has allowed life-history traits to drift towards values associated with lower fitness when following this pathway. Relaxed selection on direct development was also associated with a higher degree of genetic variation for protandry expressed as within-family sexual dimorphism in growth rate. Genetic correlations for larval growth rate across sexes and pathways were generally positive, with the notable exception of correlation estimates that involved directly developing males of the population that experienced relaxed selection on this pathway. We conclude that relaxed selection on one developmental pathway appears to have partly disrupted the developmental regulation of life-history trait expression. This in turn suggests that ongoing selection may be responsible for maintaining adaptive developmental regulation along alternative developmental pathways in these populations.     

Food selection in three leaf-shredding stream invertebrates

Leaf disks (Betula papyrifera) were conditioned for two weeks by six species of aquatic hyphomycetes. Mass losses of the leaves were determined, and their concentrations of protein (extracted at pH 7, 10 and 12.8), phenolics (Folin-Ciocalteu and BSA-precipitation), lipids, and ergosterol (as indicator of fungal biomass) were measured. Enzymatic activities of the culture filtrates against cellulose, xylan and pectin were estimated. Gammarus tigrinis, Pycnopsyche guttifer and Tipula caloptera were given a choice of the six leaf/fungus combinations. G. tigrinus and P. guttifer consistently preferred some combinations over others; T. caloptera appeared to feed randomly. There were no significant correlations between consumption and any of the measured characteristics of leaf disks. With G. tigrinus and P. guttifer, the sequence of preference could be reproduced by extracting mycelia with non-polar solvents and applying the extracts to unconditioned leaf disks. Consumption of extract-coated disks was lower than consumption of conditioned disks. Numbers of endosymbiotic gut bacteria increased from G. tigrinus to P. guttifer to T. caloptera; diet diversity showed the opposite trend.