Exploring sub-lethal effects of exposure to a nucleopolyhedrovirus in the speckled wood (Pararge aegeria) butterfly

This study investigated the sub-lethal effects of larval exposure to baculovirus on host life history and wing morphological traits using a model system, the speckled wood butterfly Pararge aegeria (L.) and the virus Autographa californica nucleopolyhedrovirus. Males and females showed similar responses to the viral infection. Infection significantly reduced larval growth rate, whilst an increase in development time allowed the critical mass for pupation to be attained. There was no direct effect of viral infection on the wing morphological traits examined. There was, however, an indirect effect of resisting infection; larvae that took longer to develop had reduced resource investment in adult flight muscle mass.     

Morphological variation of <Emphasis Type="Italic">Melanargia russiae</Emphasis> (Esper, 1783) (Lepidoptera,Satyridae) from the main part of the range and in case of its expansion to the north under climate change conditions

A climate-related shift in the range boundaries of the western–central Eurasian subboreal species Melanargia russiae in the Ural region from the northern forest-steppe zone to pine–birch forests was found. Morphological variation of M. russiae wings from the boundary northern populations and populations from the main part of the range in the Urals were studied. The results of a complex analysis of the morphological traits (size, wing shape, and wing pattern eyespots) confirm the hypothesis that the local population formed in the south of Sverdlovsk oblast and contradict the hypothesis of the migratory origin of M. russiae imago.     

Pathways to fitness: carry‐over effects of late hatching and urbanisation on lifetime mating success

Life history theory and most empirical studies assume carry‐over effects of larval ­conditions to shape adult fitness through their impact on metamorphic traits (age and mass at metamorphosis). Yet, very few formal tests of this connection across metamorphosis exist, because this entails longitudinal studies from the egg stage and requires measuring fitness in (semi)natural conditions. In a longitudinal one‐year common‐garden rearing experiment consisting of an outdoor microcosm part for the larval stage and a large outdoor insectary part for the adult stage, we studied the effects of two factors related to time constraints in the larval stage (egg hatching period and urbanisation) on life history traits and lifetime mating success in the males of the damselfly Coenagrion puella. We reared early‐ and late‐hatched larvae from each of three rural and three urban populations from the egg stage throughout their adult life. Key findings were that both the hatching period and urbanisation shaped adult fitness, yet through different pathways. As expected, the more time‐constrained late‐hatched individuals accelerated their larval life history and this was associated with a lower lifetime mating success. A path analysis revealed this carry‐over effect was mediated by the changes in the two metamorphic traits (reduced age and lower mass at emergence). Notably, urban males had a 50% lower lifetime mating success, which was not mediated by age and mass at emergence, and possibly driven by their shorter lifespan. Our results point to long‐term carry‐over effects of the usually ignored natural variation in egg hatching dates, and further contribute to the limited evidence showing fitness costs of adjusting to an urban lifestyle.     

Drivers of wing shape in a widespread Neotropical bird: a dual role of sex-specific and migration-related functions

A large body of research has shown how avian morphology is shaped by specific behavioral repertoires and life history traits. Yet, the majority of such research has been conducted on birds breeding at north-temperate latitudes. We tested the hypothesis that functional wing traits of Fork-tailed Flycatchers (Tyrannus savana), which migrate within South America, vary predictably between non-migratory and migratory flycatchers. Additionally, due to sex-specific differences in this species (e.g., males perform courtship displays), we explored sex-related variation in wing shape. We applied classic measures of wing shape (e.g., wing loading, length, aspect ratio, pointedness), as well as landmark-based morphometric analysis to describe the wing morphology of Fork-tailed Flycatchers from breeding populations across South America. We found that migratory flycatchers tend to have more pointed wings than non-migratory flycatchers. Additionally, we found that males have wings that are significantly longer, more pointed, with a higher aspect ratio and that are more swept than those of females, regardless of whether they migrate or not. Overall, our results suggest that wing shape of Fork-tailed Flycatchers is the result of a complex set of tradeoffs shaped by selective pressures exerted on both sexes (i.e., the need to forage on the wing, evade predators and migrate efficiently), as well as sex-specific behaviors (e.g., the need for males to execute acrobatic displays).     

Thermal evolution of pre-adult life history traits, geometric size and shape, and developmental stability in Drosophila subobscura

Replicated lines of Drosophila subobscura originating from a large outbred stock collected at the estimated Chilean epicentre (Puerto Montt) of the original New World invasion were allowed to evolve under controlled conditions of larval crowding for 3.5 years at three temperature levels (13, 18 and 22 degrees C). Several pre-adult life history traits (development time, survival and competitive ability), adult life history related traits (wing size, wing shape and wing-aspect ratio), and wing size and shape asymmetries were measured at the three temperatures. Cold-adapted (13 degrees C) populations evolved longer development times and showed lower survival at the highest developmental temperature. No divergence for wing size was detected following adaptation to temperature extremes (13 and 22 degrees C), in agreement with earlier observations, but wing shape changes were obvious as a result of both thermal adaptation and development at different temperatures. However, the evolutionary trends observed for the wing-aspect ratio were inconsistent with an adaptive hypothesis. There was some indication that wing shape asymmetry has evolutionarily increased in warm-adapted populations, which suggests that there is additive genetic variation for fluctuating asymmetry and that it can evolve under rapid environmental changes caused by thermal stress. Overall, our results cast strong doubts on the hypothesis that body size itself is the target of selection, and suggest that pre-adult life history traits are more closely related to thermal adaptation.     

Integrative approach revealed contrasting pattern of spatial structuring within urban and rural biotypes of Culex pipiens

Population structure of pests is an important issue when designing management strategies to optimize control measures. In this study, we investigated a spatial pattern of genetic and phenotypic variation within seven urban and within six rural populations of Culex pipiens from Vojvodina Province (Serbia) incorporating landscape genetic methods (using allozyme data) and wing size and shape (using geometric morphometric approach). Comparing rural samples, no strong genetic groupings of individuals were detected. Nevertheless, traditional approaches where individuals are pre‐assigned to populations, including F statistics and amova (analysis of molecular variance), revealed low, but significant genetic differentiation among samples. Similarly, phenotypic data (wing size and shape) indicated some level of heterogeneity among rural samples. Contrary to genetic homogeneity found within rural biotype, the individual‐based structuring characterized urban biotype. Geneland revealed the presence of two genetic clusters within urban group which is in concordance with F_ST and amova results. These results showed that sample from Novi Sad (NS) is a distinct genetic unit, which has been likely resulted in intensive insecticide use over several decades. Furthermore, phenotypic differentiation supported the existence of spatial structuring. Therefore, complementary use of molecular markers and phenotypic traits may be a powerful tool for revealing hidden spatial diversity within Cx. pipiens.     

Coevolution of traits determining migratory tendency: correlated response of a critical enzyme,juvenile hormone esterase,to selection on wing morphology

Migratory tendency in insects is a complex trait, composed of a suite of correlated behavioural, physiological, morphological and life history traits. We investigate the genetic and physiological basis of the coevolution of this suite of traits using laboratory lines of the wing dimorphic cricket, Gryllus firmus, selected for increasing and decreasing incidence of macroptery. Selection on wing morphology has produced strong direct responses in proportion macropterous as well as correlated (indirect) responses in wing muscle histolysis, flight propensity and fecundity. We investigate the hypothesis that these responses have been mediated by changes in the metabolism of juvenile hormone (JH) during the final nymphal stadium (the critical period for wing morph determination). Previous studies of Gryllus sp. have established that JH titre in this period is determined primarily by the activity of the degradative enzyme, juvenile hormone esterase (JHE). Assays of JHE activity in the final nymphal stadium of the replicated control and selected lines demonstrate highly significant differences in both mean activity and the probability of macroptery for a given level of activity (i.e., the threshold activity required to induce wing formation). These correlated responses in JH metabolism support the general hypothesis that the correlations among traits determining migratory tendency result at least in part from the common influence of JH during the final nymphal stadium. We discuss these results in the context of the quantitative genetic model for the evolution of polygenic, dichotomous traits (the threshold model), and present four general predictions concerning the coevolution of traits associated with ecological (i.e., trophic, life history, behavioural) dimorphisms.     

Genetic and maternal influences on life history plasticity in milkweed bugs (Oncopeltus): response to temperature

This study was designed to examine life history flexibility arising from phenotypic plasticity in response to temperature and from maternal effects in response to reproductive diapause in a temperate zone population of the milkweek bug (Oncopeltus fasciatus). We employed a split-family, first-cousin, full-sib design with siblings reared at different temperatures in order to quantify phenotypic plasticity, maternal effects, and variation for each. The following traits were analyzed: development time, age at first reproduction, longevity, early-life fecundity, and wing length. We found both life history plasticity and maternal effects on life history traits which tend to enhance the colonizing ability of offspring born to mothers that have undergone reproductive diapause. We were unable to demonstrate additive genetic variation for plasticity for any of the traits, while for development time and wing length we found variation due to non-additive genetic or common-environmental sources. We were also unable to demonstrate additive genetic variation for maternal effects, although variation may exist at low levels that are difficult to detect using cousin-families. The apparent lack of variation in this population would constrain evolution of life history flexibility even though considerable flexibility exists in the phenotype.     

Developmental plasticity and acclimation both contribute to adaptive responses to alternating seasons of plenty and of stress in <Emphasis Type="Italic">Bicyclus</Emphasis> butterflies

Plasticity is a crucial component of the life cycle of invertebrates that live as active adults throughout wet and dry seasons in the tropics. Such plasticity is seen in the numerous species of Bicyclus butterflies in Africa which exhibit seasonal polyphenism with sequential generations of adults with one or other of two alternative phenotypes. These differ not only in wing pattern but in many other traits. This divergence across a broad complex of traits is associated with survival and reproduction either in a wet season that is favourable in terms of resources, or mainly in a dry season that is more stressful. This phenomenon has led us to examine the bases of the developmental plasticity in a model species, B. anynana, and also the evolution of key adult life history traits, including starvation resistance and longevity. We now understand something about the processes that generate variation in the phenotype, and also about the ecological context of responses to environmental stress. The responses clearly involve a mix of developmental plasticity as cued by different environments in pre-adult development, and the acclimation of life history traits in adults to their prevailing environment.     

Fruit type,life form and origin determine the success of woody plant invaders in an urban landscape

The spread of alien plant species is a critical ecological event worldwide, but the forces that control this spread are not well documented. Alien plant species are well known to disrupt ecological services of native ecosystems, change the composition of native habitats, and often lead to the extirpation of native flora and fauna. Here, we report on life history patterns of plant species with rapidly spreading and declining ranges in North America’s major urban region. We tested for differences in life history traits between the 466 native and alien woody flora of the New York metropolitan area. We also examined the relationship between life history traits and change in distribution in the New York metropolitan area between 1900 and 2000. Native and alien species of the New York metropolitan area differ with respect to pollination vector and breeding system. However, pollination vector and breeding system are not associated with success, defined here as increasing range spread in the urban environment; instead, fruit type (dispersal), life form and origin are important determinants of success. Alien species that are deciduous trees, shrubs or vines with fleshy fruit are the most successful in increasing their distribution in this urban landscape. Newly introduced species with these characteristics are expected to have a better chance at establishing in similar urban landscapes and should be targets for intensive management. The ability to predict which alien species will become invasive is also a valuable tool for the prevention of invasions by newly introduced plant species.     

Formation of melanin-based wing patterns is influenced by condition and immune challenge in Pieris brassicae

According to life‐history theory, trade‐offs emerge because organisms possess a limited amount of resources that they have to allocate between different bodily functions. Here, we tested whether there is a trade‐off between melanin‐based immune response and dark melanized wing patterning in the large white butterfly, Pieris brassicae L. (Lepidoptera: Pieridae), by activating the immune system of pupae and measuring the wing pigmentation of freshly emerged adults. In contrast to expectations, we did not find any negative associations between immune challenge and wing patterning. Furthermore, implanted and punctured male pupae tended to have larger and darker forewing tips as adults compared to controls. Both in females and males, different wing spots were affected by condition‐reflecting traits (e.g., pupal mass, brood), which suggest that formation of wing patterns may be a condition‐dependent process and/or heritable.     

Extensive gene flow along the urban–rural gradient in a migratory colonial bird

Urban colonization by wildlife involves a combination of several different mechanisms, including phenotype or genotype sorting, phenotypic plasticity and microevolutionary adaptation. Combination of these processes can produce a rapid phenotypic, but also genetic divergence of urban versus rural populations. Here, we examined the pattern of genetic differentiation between urban and rural populations of a colonial migratory bird, the black‐headed gull Chroicocephalus ridibundus. To this end, we sampled ca 170 individuals from six (two urban and four rural) colonies in northern Poland, and genotyped them at ten microsatellite loci. Our analysis provided evidence for negligible genetic divergence of urban and rural colonies, as assessed with fixation index F_ST and Nei's unbiased genetic distance D (mean pairwise urban‐rural comparisons: F_ST = 0.003 ± 0.001 [SE] and D = 0.012 ± 0.006 [SE]). Bayesian clustering methods provided support for homogeneous genetic structure across all urban and rural populations. Also, we found no support for reduced allelic diversity in urban versus rural colonies. These results stand in a stark contrast to the previous findings on the genetic consequences of urbanization in birds. We hypothesize that this pattern could possibly be attributed to the important life‐history characters of the black‐headed gull, including coloniality, migratoriness, and high dispersal propensity. Our study provides a novel insight into the urban landscape genetics, underlining large variation in the mechanisms of urban colonization and its genetic consequences in wild animal populations.     

Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment

Adult fitness components may strongly depend on variation in locomotory performance such as flight; this variation can be sex specific. Fast take-off to intercept females and competing males is an essential behavioral component of the territorial perching behavior in male speckled wood butterflies (Pararge aegeria L.). Females on the other hand avoid frequent take-offs particularly under suboptimal temperatures, typically showing fewer but longer flights than males. We estimated the heritability of take-off acceleration performance under suboptimal body temperatures by a restricted maximum-likelihood model. We calculated genetic correlations between this performance and a selection of morphological traits: size (body mass), flight muscle investment (relative thorax mass), and wing shape (forewing aspect ratio). Our results show significant additive genetic variation for mean acceleration performance and a similar but nonsignificant trend (P= 0.08) for maximal acceleration performance during take-off in males (h(2)= 0.15). In females, heritability was not significantly different from zero for either of the acceleration performance measures. Morphological traits and take-off performance were genetically linked in a sex-specific way. In males, relative thorax mass and forewing aspect ratio were positively genetically correlated with acceleration performance. In females, there was a negative genetic correlation between acceleration performance and abdomen mass, but not with residual abdomen mass (i.e., regressed on total body mass). To fully understand the evolution of sexual differences in flight performances and morphology, several other flight performances will have to be included. This multifunctional nature of flight and its consequences for the evolutionary study of flight has not yet been fully appreciated in the literature.     

The costs of being dark: the genetic basis of melanism and its association with fitness‐related traits in the sand cricket

Melanism is an important component of insect cuticle and serves numerous functions that enhance fitness. Despite its importance, there is little information on its genetic basis or its phenotypic and genetic correlation with fitness‐related traits. Here, we examine the heritability of melanism in the wing dimorphic sand cricket and determine its phenotypic and genetic correlation with wing morphology, gonad mass and size of the dorso‐longitudinal muscles (the principle flight muscles). Previously demonstrated trade‐offs among these traits are significant factors in the evolution of life history variation. Using path analysis, we show that melanization is causally related to gonad mass, but not flight muscle mass. Averaged over the sexes, the heritability of melanism was 0.61, the genetic correlation with gonad mass was ?0.36 and with wing morph was 0.51. The path model correctly predicted the ranking of melanization score in lines selected for increased ovary mass, increased flight muscle mass, an index that increased both traits and an unselected control. Our results support the general hypothesis that melanization is costly for insects and negatively impacts investment in early reproduction.     

Intermolt development reduces oxygen delivery capacity and jumping performance in the American locust (<Emphasis Type="Italic">Schistocerca americana</Emphasis>)

Among animals, insects have the highest mass-specific metabolic rates; yet, during intermolt development the tracheal respiratory system cannot meet the increased oxygen demand of older stage insects. Using locomotory performance indices, whole body respirometry, and X-ray imaging to visualize the respiratory system, we tested the hypothesis that due to the rigid exoskeleton, an increase in body mass during the intermolt period compresses the air-filled tracheal system, thereby, reducing oxygen delivery capacity in late stage insects. Specifically, we measured air sac ventilation frequency, size, and compressibility in both the abdomen and femur of early, middle, and late stage sixth instar Schistocerca americana grasshoppers. Our results show that late stage grasshoppers have a reduced air sac ventilation frequency in the femur and decreased convective capacities in the abdomen and femur. We also used X-ray images of the abdomen and femur to calculate the total proportion of tissue dedicated to respiratory structure during the intermolt period. We found that late stage grasshoppers had a lower proportion of their body dedicated to respiratory structures, especially air sacs, which convectively ventilate the tracheal system. These intermolt changes make oxygen delivery more challenging to the tissues, especially critical ones such as the jumping muscle. Indeed, late stage grasshoppers showed reduced jump frequencies compared to early stage grasshoppers, as well as decreased mass-specific CO₂ emission rates at 3 kPa PO₂. Our findings provide a mechanism to explain how body mass changes during the intermolt period reduce oxygen delivery capacity and alter an insect’s life history.     

The effect of habitat amount on flight-related traits in the butterfly Hamadryas februa is sex-dependent

1. Mobility in flying animals can be assessed by variations in morpho–ecological traits such as body, thorax and wing sizes, wing shape and the proportion between body mass and wing area. Habitat loss and fragmentation can promote phenotypic plasticity and microevolutionary divergencies in natural populations. In this context, sexual differences in physiology and behaviour can impose different selection pressure on morphological aspects related to flight.
2. We evaluated the relative impact of forest patch area and habitat amount in shaping flight-related morpho–ecological traits of the tropical butterfly Hamadryas februa. We find a marked sexual dimorphism in the species, with females being larger, having larger thorax, higher wing loadings and larger wing total area than males. These trait values indicate females as the more dispersive sex. We show that habitat amount modulates body mass allocations in both sexes, leading to an increase in thorax mass with decreasing habitat amount. The effect of habitat amount was more pronounced in females, which increased total mass and wing loading while decreasing thorax allocation with decreasing habitat amount. This outcome suggests that females increase abdominal mass in response to a reduction in habitat amount. The focal forest patch increasing area was linked to increases in hindwing lengths in both females and males.
3. We advocate that both landscape metrics (i.e., habitat amount and patch area) should be considered in studies evaluating landscapes' impacts on insect mobility. We discuss results in terms of the species' sexual differences in flight behaviour and the relative importance of both landscape metrics.

     

Urbanization disrupts latitude‐size rule in 17‐year cicadas

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.     

Flight morphology corresponds to both surrounding landscape structure and local patch conditions in a highly specialized peatland butterfly (Lycaena epixanthe)

1. Movement mediates the response of populations and communities to landscape and habitat spatial structure, yet movement capability may itself be modified by selection pressures accompanying landscape change. Insect flight morphology can be affected by both the landscape surrounding habitat patches and the distribution of resources within habitat patches. 2. This study investigated the relative influence of local habitat patch conditions and surrounding landscape structure on variation in morphological traits associated with flight in the bog copper (Lycaena epixanthe), a butterfly endemic to temperate Nearctic peatlands. 3. Eight habitat patches were sampled to assess the influence of the surrounding landscape (connectivity of potential habitat and matrix composition) and patch size (an integrated proxy of resource density and spatial distribution) on investment into flight, measured by thorax and abdomen mass, and wing area. 4. The results revealed an effect of both local habitat conditions and landscape structure on flight‐related morphological traits. Increasing forest cover in the surrounding landscape, indicative of increased habitat patch isolation, corresponded with less mobile phenotypes in both sexes. Surrounding landscapes with more water were also generally associated with less mobile phenotypes. Investment into flight was greater in smaller peatlands in which host plant density is higher and more homogeneously distributed. 5. The present study highlights that morphological traits associated with mobility may be responding to both local habitat patch characteristics and surrounding landscape structure. It also supports the hypothesis that local habitat conditions contribute to morphological variation in butterflies.     

Matching field and laboratory environments: effects of neglecting daily temperature variation on insect reaction norms

The tropical butterfly, Bicyclus anynana, exhibits seasonal polyphenism. The wet season form has large eyespots and a pale band while these characters are much less conspicuous or absent in the dry season form. This plasticity is induced in the laboratory by use of a standard series of constant temperatures in the larval stage yielding a continuous norm of reaction. Butterflies in this study were reared from hatchling larvae in seven regimes which differed with respect to thermoperiod or photoperiod. The effect of rearing treatment on the phenotypic plasticity of the adult wing pattern, on life history traits and on larval feeding rhythms was investigated. Photoperiod had little effect except that constant light produced a higher mortality and tended to produce a longer development time. Thermoperiod had a major effect on the life history traits in comparison to a constant temperature regime with the same daily mean: development time was shorter with higher growth rates. The faster development was associated with a substantial shift in the wing pattern towards the wet season form. Larvae feed mostly at night both under constant and thermoperiod (cool nights) conditions. The results are discussed with respect to the necessity of matching field and laboratory environments in studies of norms of reaction or of life history traits where the adaptive significance of the variation is important. Fluctuating conditions in nature, especially with respect to thermoperiod, must be taken into account.     

The Mass-Longevity Triangle: Pareto Optimality and the Geometry of Life-History Trait Space

When organisms need to perform multiple tasks they face a fundamental tradeoff: no phenotype can be optimal at all tasks. This situation was recently analyzed using Pareto optimality, showing that tradeoffs between tasks lead to phenotypes distributed on low dimensional polygons in trait space. The vertices of these polygons are archetypes—phenotypes optimal at a single task. This theory was applied to examples from animal morphology and gene expression. Here we ask whether Pareto optimality theory can apply to life history traits, which include longevity, fecundity and mass. To comprehensively explore the geometry of life history trait space, we analyze a dataset of life history traits of 2105 endothermic species. We find that, to a first approximation, life history traits fall on a triangle in log-mass log-longevity space. The vertices of the triangle suggest three archetypal strategies, exemplified by bats, shrews and whales, with specialists near the vertices and generalists in the middle of the triangle. To a second approximation, the data lies in a tetrahedron, whose extra vertex above the mass-longevity triangle suggests a fourth strategy related to carnivory. Each animal species can thus be placed in a coordinate system according to its distance from the archetypes, which may be useful for genome-scale comparative studies of mammalian aging and other biological aspects. We further demonstrate that Pareto optimality can explain a range of previous studies which found animal and plant phenotypes which lie in triangles in trait space. This study demonstrates the applicability of multi-objective optimization principles to understand life history traits and to infer archetypal strategies that suggest why some mammalian species live much longer than others of similar mass.