Rapid evolution of larval life history,adult immune function and flight muscles in a poleward‐moving damselfly

Although a growing number of studies have documented the evolution of adult dispersal‐related traits at the range edge of poleward‐expanding species, we know little about evolutionary changes in immune function or traits expressed by nondispersing larvae. We investigated differentiation in larval (growth and development) and adult traits (immune function and flight‐related traits) between replicated core and edge populations of the poleward‐moving damselfly Coenagrion scitulum. These traits were measured on individuals reared in a common garden experiment at two different food levels, as allocation trade‐offs may be easier to detect under energy shortage. Edge individuals had a faster larval life history (growth and development rates), a higher adult immune function and a nearly significant higher relative flight muscle mass. Most of the differentiation between core and edge populations remained and edge populations had a higher relative flight muscle mass when corrected for latitude‐specific thermal regimes, and hence could likely be attributed to the range expansion process per se. We here for the first time document a higher immune function in individuals at the expansion front of a poleward‐expanding species and documented the rarely investigated evolution of faster life histories during range expansion. The rapid multivariate evolution in these ecological relevant traits between edge and core populations is expected to translate into changed ecological interactions and therefore has the potential to generate novel eco‐evolutionary dynamics at the expansion front.     

Sex,life history and morphology drive individual variation in flight performance of an insect parasitoid

1. The movement of organisms can be driven by multiple factors and has implications for fitness and the spatial distribution of populations. Insects spend a large proportion of their adult lives foraging by flying for resources; however, their capability and motivation to move can vary across individuals. 2. The aims of this study were to examine interindividual and sex differences in flight performance and flight characteristics, using a flight mill bioassay, in Megarhyssa nortoni (Hymenoptera; Ichneumonidae), a parasitoid of the invasive woodwasp Sirex noctilio (Hymenoptera: Siricidae), one of the most important pests of pine afforestation worldwide. We also assessed the influence of morphological traits in combination with sex on flight and explored the cost of flight on longevity and mass loss. 3. The results show a difference between sexes in flight characteristics and performance. Females show greater total distance flown than males, and have a better capacity to undergo sustained flight. Sexual size dimorphism was also found and it was noted that size positively affects distances travelled. Females have a longer life span than males, yet no differences were noted in longevity within sex between individuals that did not fly and those that flew. Age did not influence flight performance of females or impacted on post‐flight longevity. Females lost less body mass than males even after flying longer distances. 4. These results suggest that sex‐specific behaviours probably govern flight abilities together with (and not only because of) morphological traits. The paper discusses sex‐specific life‐history strategies in parasitoids and their implications for biocontrol programmes.     

Trade-off between flight activity and life-history components in Chrysoperla sinica

We studied the effects of flight duration on two important life-history traits, i.e., longevity and life-time egg production, of Chrysoperla sinica females, through an experimental flight manipulation bioassay, using a flight mill apparatus. In addition, we assessed the potential transgenerational effects of maternal flight durations on survival and on the development of the progeny. We found experimental evidence of a negative link between flight activity (1, 2 and 3 h) and longevity and reproductive activity in C. sinica females. Although, the development of the progeny 1st instars was significantly longer for females that flew longer, all other recorded life history traits of the progeny, including juvenile survival and overall development time and size of the pupae, were not affected. Hence, these findings suggest that the growth of new populations originated by females that flew long distances maybe be slower only for the first generation.     

Influence of Developmental Conditions on Immune Function and Dispersal-Related Traits in the Glanville Fritillary (Melitaea cinxia) Butterfly

Organisms in the wild are constantly faced with a wide range of environmental variability, such as fluctuation in food availability. Poor nutritional conditions influence life-histories via individual resource allocation patterns, and trade-offs between competing traits. In this study, we assessed the influence of food restriction during development on the energetically expensive traits flight metabolic rate (proxy of dispersal ability), encapsulation rate (proxy of immune defence), and lifespan using the Glanville fritillary butterfly, Melitaea cinxia, as a model organism. Additionally, we examined the direct costs of flight on individual immune function, and whether those costs increase under restricted environmental conditions. We found that nutritional restriction during development enhanced adult encapsulations rate, but reduced both resting and flight metabolic rates. However, at the individual level metabolic rates were not associated with encapsulation rate. Interestingly, individuals that were forced to fly prior to the immune assays had higher encapsulation rates than individuals that had not flown, suggesting that flying itself enhances immune response. Finally, in the control group encapsulation rate correlated positively with lifespan, whereas in the nutritional restriction group there was no relationship between these traits, suggesting that the association between encapsulation rate on adult lifespan was condition-dependent. Thus stressful events during both larval development (food limitation) and adulthood (forced flight) induce increased immune response in the adult butterflies, which may allow individuals to cope with stressful events later on in life.     

A Genetic RNAi Screen for IP3/Ca2+ Coupled GPCRs in Drosophila Identifies the PdfR as a Regulator of Insect Flight

Insect flight is regulated by various sensory inputs and neuromodulatory circuits which function in synchrony to control and fine-tune the final behavioral outcome. The cellular and molecular bases of flight neuromodulatory circuits are not well defined. In Drosophila melanogaster, it is known that neuronal IP₃ receptor mediated Ca²⁺ signaling and store-operated Ca²⁺ entry (SOCE) are required for air-puff stimulated adult flight. However, G-protein coupled receptors (GPCRs) that activate intracellular Ca²⁺ signaling in the context of flight are unknown in Drosophila. We performed a genetic RNAi screen to identify GPCRs that regulate flight by activating the IP₃ receptor. Among the 108 GPCRs screened, we discovered 5 IP₃/Ca²⁺ linked GPCRs that are necessary for maintenance of air-puff stimulated flight. Analysis of their temporal requirement established that while some GPCRs are required only during flight circuit development, others are required both in pupal development as well as during adult flight. Interestingly, our study identified the Pigment Dispersing Factor Receptor (PdfR) as a regulator of flight circuit development and as a modulator of acute flight. From the analysis of PdfR expressing neurons relevant for flight and its well-defined roles in other behavioral paradigms, we propose that PdfR signaling functions systemically to integrate multiple sensory inputs and modulate downstream motor behavior.     

Predicting the sensitivity of butterfly phenology to temperature over the past century

Studies to date have documented substantial variation among species in the degree to which phenology responds to temperature and shifts over time, but we have a limited understanding of the causes of such variation. Here, we use a spatially and temporally extensive data set (ca. 48 000 observations from across Canada) to evaluate the utility of museum collection records in detecting broad‐scale phenology‐temperature relationships and to test for systematic differences in the sensitivity of phenology to temperature (days °C^?1) of Canadian butterfly species according to relevant ecological traits. We showed that the timing of flight season predictably responded to temperature both across space (variation in average temperature from site to site in Canada) and across time (variation from year to year within each individual site). This reveals that collection records, a vastly underexploited resource, can be applied to the quantification of broad‐scale relationships between species' phenology and temperature. The timing of the flight season of earlier fliers and less mobile species was more sensitive to temperature than later fliers and more mobile species, demonstrating that ecological traits can account for some of the interspecific variation in species' phenological sensitivity to temperature. Finally, we found that phenological sensitivity to temperature differed across time and space implying that both dimensions of temperature will be needed to translate species' phenological sensitivity to temperature into accurate predictions of species' future phenological shifts. Given the widespread temperature sensitivity of flight season timing, we can expect long‐term temporal shifts with increased warming [ca. 2.4 days °C^?1 (0.18 SE)] for many if not most butterfly species.     

Sexual dimorphism and growth trade‐offs in Blue Tit Cyanistes caeruleus nestlings

The outcome of sibling competition for food is often determined by variation in body size within the brood and involves trade‐offs; traits that enhance competitive ability within the nest may be developed at the expense of traits that enable effective flight at fledging, or vice versa. We quantified growth of skeletal, body mass and feather traits in male and female Blue Tit Cyanistes caeruleus nestlings. Males were significantly heavier, had longer tarsi and tended to have greater head–bill lengths than females, whereas females were similar to males in wing flight feather growth. These differences in growth may result from sexual differences in selection of the traits. Females are likely to prioritize feather growth to facilitate synchronized fledging with the rest of the brood, and to enhance escape from predators. We suggest that males are heavier and develop longer tarsi because body size is an important determinant of male reproductive success.     

Interrelations of global macroecological patterns in wing and thorax size,sexual size dimorphism,and range size of the Drosophilidae

Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r² = 0.05) and wing size (r² = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r² = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r² = 0.14). Yet, this pattern was largely driven by the virilis–repleta radiation. Finally, range size did not correlate with latitude, although a positive relationship was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.     

Variations in life history traits and flight capacity among populations of the light brown apple moth Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae)

Abstract The empirical study of interpopulation variation in life history and other fitness traits has been an important approach to understanding the ecology and evolution of organisms and gaining insight into possible sources of variation. We report a quantitative analysis for variations of five life history traits (larval developmental time, adult body weight, adult lifespan, age at first reproduction, total fecundity) and flight capacity among populations of Epiphyas postvittana originating from four localities in Australia and one in New Zealand. These populations were compared at two temperatures (15° and 25°C) after being maintained under uniform laboratory conditions for 1.5 generations, so that the relative role of genetic divergence and phenotypic plasticity in determining interpopulation variation could be disentangled. Genetic differentiation between populations was shown in all measured traits, with the greatest divergence occurring in developmental time, fecundity and adult body size. However, these traits were highly sensitive to changes in environmental temperatures; and furthermore, significant interactions between population and temperature occurred in all traits except for flight capacity of female moths. Thus, phenotypic plasticity may be another cause of interpopulation variation. The interpopulation variation for some measured traits was apparently related to climatic differences found where the populations originated. Individuals of the populations from the warmer climates tended to develop more slowly at immature stages, producing smaller and less fecund moths but with stronger flight capacity, in comparison to those from the cooler regions. It seems, therefore, that natural populations of E. postvittana have evolved different strategies to cope with local environmental conditions.     

The chemical basis of mate recognition in two parasitoid wasp species of the genus Nasonia

Triatomines (Hemiptera: Reduviidae) are vectors of Trypanosoma cruzi Chagas, the etiological agent of Chagas's disease. They display pre‐adult development delay – that is, a development time much longer than on average – which usually has been considered as a maladaptive trait. However, this hypothesis has not been tested. We carried out an experiment under controlled laboratory conditions to (1) test whether a development delay exists in the fifth nymphal stage of Rhodnius prolixus Stål (Hemiptera: Reduviidae, Rhodniini), and (2) measure any fitness cost related to such delay by estimating the relationship between individual development time and other life‐history traits. We analyzed the development time with various continuous statistical distributions (normal, log‐normal, Weibull, gamma, Pareto, Burr, and log‐logistic). Using goodness‐of‐fit tests, the best fit was obtained with asymmetrical distributions, with the Burr distribution showing the best fit to the data. We concluded that a development delay exists in stage five of R. prolixus without fitness cost. The combination of our results and previous work suggests that such a delay could be viewed as an adaptive response to environmental stochasticity and/or density‐dependence rather than as a maladaptive trait. We propose further investigations to provide a conclusive test of adaptive delay in triatomines.     

Genetic and phenotypic variation for flight ability in the cactophilicDrosophila species,D. aldrichi andD. buzzatii

The flight ability ofDrosophila aldrichi (Patterson & Crow) andD. buzzatii (Patterson & Wheeler) using tethered flights, was measured with respect to age-related changes, genetic variation and adult body size variation induced by rearing at different larval densities.Drosophila buzzatii flew for much longer thanD. aldrichi, especially females, but age-related changes in flight duration were significant only forD. aldrichi. Effects of body size on flight ability were significant inD. buzzatii, but not inD. aldrichi. InD. buzzatii, there was a significant genotype-environment interaction (larval density × line) for flight duration, with short and average flight duration isofemale lines showing longer flights, but a long flight duration line shorter flights as body size decreased (i.e., as larval density increased). Heritability estimates for flight duration were similar in the two species, but flight duration showed no significant genetic correlations with developmental time, body size or wing dimensions (except for one wing dimension inD. buzzatii). Although not significantly different between the species, heritabilities for life-history traits (adult size and developmental time) showed contrasting patterns — with higher heritability for body size (body weight and thorax length) inD. buzzatii, and higher for developmental time inD. aldrichi. In agreement with limited previous field evidence,D. buzzatii is better adapted for colonization than isD. aldrichi.     

The scaling of eye size with body mass in birds

We developed a simple method that uses skulls to estimate the diameter, and hence the mass, of birds'' eyes. Allometric analysis demonstrated that, within five orders (parrots, pigeons, petrels, raptors and owls) and across 104 families of flying birds, eye mass is proportional to (body mass)^0.68 over a range of body masses (6 g to 11.3 kg). As expected from their habits and visual ecology, raptors and owls have enlarged eyes, with masses 1.4 and 2.2 times greater than average birds of the same weight. Taking existing relationships for flight speed on body mass, we find that resolution increases close to (flight speed)^1.333. Consequently, large birds resolve objects at a longer time to contact than small birds. Eye radius and skull size co-vary in strict proportion, suggesting common physiological, aerodynamic and mechanical constraints. Because eye mass scales close to brain mass, metabolic rate and information processing could also be limiting, but the precise factors determining the scaling of eye to body have not been identified.     

Integrating large‐scale geographic patterns in flight morphology,flight characteristics and sexual selection in a range‐expanding damselfly

While geographic trait variation along environmental clines is widespread, associated patterns in sexual selection remain largely unexplored. Geographic patterns in sexual selection may be expected if 1) phenotypes vary geographically and sexual selection is dependent on the local phenotypes in the population, and if 2) sexual selection is influenced by geographically structured environmental conditions. We quantified geographic variation in flight‐related traits and flight performance in mated and unmated males and tested for geographic variation in sexual selection on these traits in the poleward range‐expanding damselfly Coenagrion scitulum across a set of eleven core and edge populations ordered along thermal gradients in the larval and in the adult stage. We found little support for trait differentiation between core and edge populations, instead we found considerable geographic trait variation along the larval and adult thermal gradients. As expected under time constraints, body mass decreased with shorter larval growth seasons. Lower temperatures during the adult flight period were associated with a higher body mass, a higher flight speed and a higher fat content; these traits likely evolved to buffer flight ability at suboptimal temperatures and to optimize starvation resistance. Across the large geographic scale, we found a consistent higher flight duration in mated males. Instead, sexual selection for higher fat content was stronger in populations with lower adult flight temperatures and sexual selection for lower body mass acted only in edge populations. Our results indicate sexual selection on flight performance to be consistent over a large geographic scale and this despite the clear geographic patterns in sexual selection on the underlying morphological traits. Our results highlight that to fully understand the fitness implications of geographically changing trait patterns, researchers should consider the entire phenotype–performance–fitness axis and incorporate effects of geographically structured life‐stage specific environmental conditions on this axis.     

Environmental and genetic control of cold tolerance in the Glanville fritillary butterfly

Thermal tolerance has a major effect on individual fitness and species distributions and can be determined by genetic variation and phenotypic plasticity. We investigate the effects of developmental and adult thermal conditions on cold tolerance, measured as chill coma recovery (CCR) time, during the early and late adult stage in the Glanville fritillary butterfly. We also investigate the genetic basis of cold tolerance by associating CCR variation with polymorphisms in candidate genes that have a known role in insect physiology. Our results demonstrate that a cooler developmental temperature leads to reduced cold tolerance in the early adult stage, whereas cooler conditions during the adult stage lead to increased cold tolerance. This suggests that adult acclimation, but not developmental plasticity, of adult cold tolerance is adaptive. This could be explained by the ecological conditions the Glanville fritillary experiences in the field, where temperature during early summer, but not spring, is predictive of thermal conditions during the butterfly's flight season. In addition, an amino acid polymorphism (Ala‐Glu) in the gene flightin, which has a known function in insect flight and locomotion, was associated with CCR. These amino acids have distinct biochemical properties and may thus affect protein function and/or structure. To our knowledge, our study is the first to link genetic variation in flightin to cold tolerance, or thermal adaptation in general.     

The effect of photoperiod on life history and blood‐feeding activity in Aedes albopictus and Aedes aegypti (Diptera: Culicidae)

Several studies have examined how climatic variables such as temperature and precipitation may affect life history traits in mosquitoes that are important to disease transmission. Despite its importance as a seasonal cue in nature, studies investigating the influence of photoperiod on such traits are relatively few. This study aims to investigate how photoperiod alters life history traits, survival, and blood‐feeding activity in Aedes albopictus (Skuse) and Aedes aegypti (Linnaeus). We performed three experiments that tested the effects of day length on female survival, development time, adult size, fecundity, adult life span, and propensity to blood feed in Ae. albopictus and Ae. aegypti. Each experiment had three photoperiod treatments: 1) short‐day (10L:14D), 2) control (12L:12D), and 3) long‐day (14L:10D). Aedes albopictus adult females were consistently larger in size when reared in short‐day conditions. Aedes aegypti adult females from short‐day treatments lived longer and were more likely to take a blood meal compared to other treatments. We discuss how species‐specific responses may reflect alternative strategies evolved to increase survival during unfavorable conditions. We review the potential impacts of these responses on seasonal transmission patterns, such as potentially increasing vectorial capacity of Ae. aegypti during periods of shorter day lengths.     

Do exaggerated chelicerae function as weapons or genitalia in a long‐jawed spider? Functional allometric analysis yields an answer

From the elongated neck of the giraffe to the elaborate train of the peacock, extreme traits can result from natural or sexual selection (or both). The extreme chelicerae of the long‐jawed spiders (Tetragnatha) present a puzzle: do these exaggerated chelicerae function as weapons or genitalia? Bristowe first proposed that Tetragnatha chelicerae function as a holdfast because these spiders embrace chelicerae during mating. This hypothesis has remained untested until now. Here, we use functional allometry to examine how extreme chelicerae develop and perform in the long‐jawed spider Tetragnatha elongata. Similar to other Tetragnatha species, chelicerae were longer in adult males than in adult females. Overall, we confirm Bristowe's hypothesis: elongation only occurred in the adult stage. However, we propose that chelicerae function as more than a holdfast in T. elongata. Male chelicerae exhibited positive allometry, which suggests scaling as weapons rather than genitalia. However, fieldwork revealed that the operational sex ratio is female‐biased and both adult male–male competition and sexual cannibalism were rarely observed. Consequently, we propose that the positive allometry of male chelicerae may result from sexual selection to mechanically mesh with larger and more fecund females. Evidence for mechanical mesh includes multiple traits ranging from apophyses and grooves to guide teeth on the basal portion of the chelicerae. In contrast, we propose that chelicerae of females are analogous to the female peacock's tail: shortened by natural selection limiting the exaggeration of sexually selected traits. Indeed, females had increased foraging efficiency compared to males and exhibited negative cheliceral allometry. We discuss the implications for the evolution of elongated chelicerae in Tetragnatha.     

The Typical Flight Performance of Blowflies: Measuring the Normal Performance Envelope of Calliphora vicina Using a Novel Corner-Cube Arena

Despite a wealth of evidence demonstrating extraordinary maximal performance, little is known about the routine flight performance of insects. We present a set of techniques for benchmarking performance characteristics of insects in free flight, demonstrated using a model species, and comment on the significance of the performance observed. Free-flying blowflies (Calliphora vicina) were filmed inside a novel mirrored arena comprising a large (1.6 m1.6 m1.6 m) corner-cube reflector using a single high-speed digital video camera (250 or 500 fps). This arrangement permitted accurate reconstruction of the flies'' 3-dimensional trajectories without the need for synchronisation hardware, by virtue of the multiple reflections of a subject within the arena. Image sequences were analysed using custom-written automated tracking software, and processed using a self-calibrating bundle adjustment procedure to determine the subject''s instantaneous 3-dimensional position. We illustrate our method by using these trajectory data to benchmark the routine flight performance envelope of our flies. Flight speeds were most commonly observed between 1.2 ms⁻¹ and 2.3 ms⁻¹, with a maximum of 2.5 ms⁻¹. Our flies tended to dive faster than they climbed, with a maximum descent rate (−2.4 ms⁻¹) almost double the maximum climb rate (1.2 ms⁻¹). Modal turn rate was around 240°s⁻¹, with maximal rates in excess of 1700°s⁻¹. We used the maximal flight performance we observed during normal flight to construct notional physical limits on the blowfly flight envelope, and used the distribution of observations within that notional envelope to postulate behavioural preferences or physiological and anatomical constraints. The flight trajectories we recorded were never steady: rather they were constantly accelerating or decelerating, with maximum tangential accelerations and maximum centripetal accelerations on the order of 3 g.     

Larval size relative to larval feeding, cannibalism of larvae, egg or adult female size and larval–adult setal patterns among 13 phytoseiid mite species

Phytoseiid mite larvae vary in size and feeding type. We compared larval size to feeding by larvae, cannibalism of larvae by adult females, egg and adult female size and the setae lengths of larvae and adults among 13 species. There was no relationship between size of larvae and either feeding by larvae or cannibalism of larvae by adult female mites. Correlations were highest between larval size as measured by idiosoma plus extended leg lengths and adult female size of idiosoma plus extended leg lengths (r²=0.746), while next highest was larval idiosoma length and adult female idiosoma length (r²=0.662) and then larval idiosoma length and egg length (r²=0.579). Based on idiosoma length, Phytoseiulus persimilis had the largest larvae (non-feeding) among species and Euseius finlandicus had the smallest larvae (obligatory feeding). However, based on idiosoma length plus extended leg length, obligatory feeding larvae (on pollen or mites) of E. finlandicus and Euseius hibisci were largest and facultative feeding larvae (on mites) of Neoseiulus californicus and obligatory feeding larvae (on mites) of Galendromus occidentalis were the smallest. Among species with non- or facultative feeding larvae, Amblyseius andersoni and Neoseiulus barkeri had larger larvae and Typhlodromus pyri and Neoseiulus fallacis had smaller larvae when leg lengths were included in larval size. Setae lengths of larvae versus adult females (after adjustment for body sizes) showed high correlation for j6 (r²=0.942) and s4 (r²=0.854), but low correlation for larval Z4 versus adult female Z4 (r²=0.084) or Z5 (r²=0.063). Overall, larval morphological traits were most closely correlated to traits of other life stages, although for setae there were some exceptions. Differences in the functions of setae j6, s4 and Z4 in the larva versus adult female are discussed.     

QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean

The relationship between root-hair growth, acid exudation and phosphorus (P) uptake as well as the quantitative trait loci (QTLs) associated with these traits were determined for a recombinant inbred line (RIL) population derived from the cross of two contrasting common bean (Phaseolus vulgaris L.) genotypes, DOR364 and G19833, which were grown in solution culture and under field conditions with low-P availability. In the solution-culture study, root-hair density, root-hair length, H⁺ exudation and total acid exudation were measured. Substantial genotypic variability was observed for these traits and their response to P availability. The P-efficient parent G19833 had greater root-hair density, longer root-hair length, and greater exudation of H⁺ and total acid than the P-inefficient genotype DOR364. These traits segregated continuously in the RIL population, with obvious tendency of trait transgression. Genetic analysis revealed that the root traits measured had various heritabilities, with h _b ² ranging from 43.24 to 86.70%. Using an integrated genetic map developed for the population, a total of 19 QTLs associated with root hair, acid exudation and P-uptake traits were detected on 8 linkage groups. P uptake in the field was positively correlated with total acid exudation, basal root-hair length, and basal root-hair density. Acid-exudation traits were intercorrelated, as were root-hair traits. Total acid exudation was positively correlated with basal root-hair density and length. Linkage analysis revealed that some of the root-trait QTLs were closely linked with QTLs for P uptake in the field. We propose that marker-assisted selection (MAS) might be a feasible alternative to conventional screening of phenotypic root traits.