World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae)

Female gypsy moths, Lymantria dispar L., from 46 geographic strains were evaluated for flight capability and related traits. Males from 31 of the same strains were evaluated for genetic diversity using two polymorphic cytochrome oxidase I mitochondrial DNA restriction sites, the nuclear FS1 marker, and four microsatellite loci. Females capable of strong directed flight were found in strains that originated from Asia, Siberia, and the northeastern parts of Europe, but flight capability was not fixed in most strains. No flight-capable females were found in strains from the United States or southern and western Europe. Wing size and musculature were shown to correlate with flight capability and potentially could be used in predicting female flight capability. The mtDNA haplotypes broadly separated the gypsy moth strains into three groups: North American, European/Siberian, and Asian. Specific microsatellite or FS1 alleles were only fixed in a few strains, and there was a gradual increase in the frequency of alleles dominant in Asia at both the nuclear and microsatellite loci moving geographically from west to east. When all the genetic marker information was used, 94% of the individuals were accurately assigned to their broad geographic group of origin (North American, European, Siberian, and Asian), but female flight capability could not be predicted accurately. This suggests that gene flow or barriers to it are important in determining the current distribution of flight-capable females and shows the need for added markers when trying to predict female flight capability in introduced populations, especially when a European origin is suspected.     

Evaluating the life‐history trade‐off between dispersal capability and reproduction in wing dimorphic insects: a meta‐analysis

A life‐history trade‐off exists between flight capability and reproduction in many wing dimorphic insects: a long‐winged morph is flight‐capable at the expense of reproduction, while a short‐winged morph cannot fly, is less mobile, but has greater reproductive output. Using meta‐analyses, I investigated specific questions regarding this trade‐off. The trade‐off in females was expressed primarily as a later onset of egg production and lower fecundity in long‐winged females relative to short‐winged females. Although considerably less work has been done with males, the trade‐off exists for males among traits primarily related to mate acquisition. The trade‐off can potentially be mitigated in males, as long‐winged individuals possess an advantage in traits that can offset the costs of flight capability such as a shorter development time. The strength and direction of trends differed significantly among insect orders, and there was a relationship between the strength and direction of trends with the relative flight capabilities between the morphs. I discuss how the trade‐off might be both under‐ and overestimated in the literature, especially in light of work that has examined two relevant aspects of wing dimorphic species: (1) the effect of flight‐muscle histolysis on reproductive investment; and (2) the performance of actual flight by flight‐capable individuals.     

Temporary flightlessness in pre‐laying Common Eiders Somateria mollissima: are females constrained by excessive wing‐loading or by minimal flight muscle ratio?

Large body size, small wings and relatively low flight muscle mass are general attributes of flightlessness in birds, but a general analysis is lacking when considering these factors simultaneously. Common Eiders Somateria mollissima are large sea ducks characterized by short, pointed wings of low surface area. Because females fast throughout incubation, they need to accumulate large body reserves prior to laying. During this pre‐laying period, many females cannot take off, and dive when approached under still‐air conditions, whereas males take off readily when disturbed. In this paper, we examine how pre‐laying female Common Eiders fit the maximum wing‐loading ratio of Meunier, the marginal flight muscle ratio (FMR) of Marden and predictions of a general model of take‐off performance (also by Marden). Wing morphology was recorded and flight muscles were dissected from specimens collected during the pre‐laying period near one breeding colony. In addition, take‐off ability, as observed during collection, was compared with the proposed thresholds for flightlessness and outputs from the general model of take‐off performance. The results indicated that half of the pre‐laying females exceeded the wing‐loading ratio of Meunier, although all females had values above 0.160, the flight muscle ratio below which take‐off would be impossible. We suggest that wing‐loading and flight muscle ratio interact in Eiders, with higher FMR compensating for excessive wing‐loading. Nevertheless, the model of take‐off performance predicted, with reasonable accuracy, the behavioural observations under still‐air conditions. Indeed, females that were predicted to be temporarily flightless could produce a specific lift of 8.8 N/kg on average (less than the 9.8 N/kg required to overcome gravity). In contrast, the average specific lift predicted for males capable of flight was estimated to be 11.4 N/kg. These results agree with our observations that female Common Eiders are at the limit of flight capability in vertebrates.     

Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism

Many polyphenisms are examples of adaptive phenotypic plasticity where a single genotype produces distinct phenotypes in response to environmental cues. Such alternative phenotypes occur as winged and wingless parthenogenetic females in the pea aphid (Acyrthosiphon pisum). However, the proportion of winged females produced in response to a given environmental cue varies between clonal genotypes. Winged and wingless phenotypes also occur in males of the sexual generation. In contrast to parthenogenetic females, wing production in males is environmentally insensitive and controlled by the sex-linked, biallelic locus, aphicarus (api). Hence, environmental or genetic cues induce development of winged and wingless phenotypes at different stages of the pea aphid life cycle. We have tested whether allelic variation at the api locus explains genetic variation in the propensity to produce winged females. We assayed clones from an F2 cross that were heterozygous or homozygous for alternative api alleles for their propensity to produce winged offspring. We found that clones with different api genotypes differed in their propensity to produce winged offspring. The results indicate genetic linkage of factors controlling the female wing polyphenism and male wing polymorphism. This finding is consistent with the hypothesis that genotype by environment interaction at the api locus explains genetic variation in the environmentally cued wing polyphenism.     

Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsis lyrata subspecies

We examined the level of postzygotic reproductive isolation in F(1) and F(2) hybrids of reciprocal crosses between the Arabidopsis lyrata subspecies lyrata (North American) and petraea (European). Our main results are: first, the percentage of fertile pollen was significantly reduced in the F(1) and F(2) compared to the parental populations. Second, mean pollen fertility differed markedly between reciprocal crosses: 84% in the F(2) with ssp. lyrata cytoplasm and 61% in the F(2) with ssp. petraea cytoplasm. Third, 17% of the F(2) with ssp. petraea cytoplasm showed male sterility (produced less than 30 pollen grains in our subsample). The hybrids were female fertile. We used QTL mapping to find the genomic regions that determine pollen fertility and that restore cytoplasmic male sterility (CMS). In the F(2) with ssp. lyrata cytoplasm, an epistatic pair of QTLs was detected. In the reciprocal F(2) progeny, four QTLs demonstrated within-population polymorphism for hybrid male sterility. In addition, in the F(2) with ssp. petraea cytoplasm, there was a strong male fertility restorer locus on chromosome 2 where a cluster of CMS restorer gene-related PPR genes have been found in A. lyrata. Our results underline the importance of cytonuclear interactions in understanding genetics of the early stages of speciation.     

Male-specific flight apparatus development in Acyrthosiphon pisum (Aphididae, Hemiptera, Insecta): comparison with female wing polyphenism

Wing polymorphisms observed in many Insecta are important topics in developmental biology and ecology; these polymorphisms are a consequence of trade-offs between flight and other abilities. The pea aphid, Acyrthosiphon pisum, possesses 2 types of wing polymorphisms: One is a genetic wing polymorphism occurring in males, and the other is an environmental wing polyphenism seen in viviparous females. Although genetic and environmental cues for the 2 wing polymorphisms have been studied, differences in their developmental regulation have not been elucidated. In particular, there is little knowledge regarding the developmental processes in male wing polymorphism. Therefore, in this study, the development of flight apparatuses and external morphologies was compared among 3 male wing morphs (winged, wingless, and intermediate). These male developmental processes were subsequently compared with those of female wing morphs. Developmental differences between the male and female polymorphisms were identified in flight muscle development and degeneration but not in wing bud development. Furthermore, the nymphal periods of wingless and intermediate males were significantly shorter than that of winged males, indicating the adaptive significance of male winglessness. Overall, this study indicates that the male and female wing polymorphisms are based on different regulatory systems for flight apparatus development, which are probably the result of different adaptations under different selection pressures.     

Synchronous Crepuscular Flight of Female Asian Gypsy Moths: Relationships of Light Intensity and Ambient and Body Temperatures

Female gypsy moths (Lymantria dispar) of Asian heritage studied in central Siberia and Germany exhibit a highly synchronous flight at dusk, after light intensity falls to about 2 lux. This critical light intensity sets the timing of flight behaviors independent of ambient temperature. Flight follows several minutes of preflight wing fanning during which females in Germany and those from a laboratory colony (derived from Siberian stock) raised their thoracic temperatures to 32–33°C at ambient temperatures of 19–22°C. Thoracic temperature of females in free flight exceeded the air temperature (19–22°C) by approximately 11–13°C. The duration of wing fanning was strongly dependent on ambient temperature. In Germany, where ambient temperatures at dusk ranged between 21 and 25°C, females wing fanned for only 2.1 ± 0.2 (SE) min; in the much colder temperatures prevalent at dusk in Bellyk, central Siberia (11–13°C), females spent 11.2 ± 0.6 min in preflight wing fanning. The majority (80%) of mated and even virgin females initiated flight during the evening of the day they eclosed. However, in Bellyk, a small proportion (12%) of females wing fanned for an extended time but then stopped, whereas others (8%) never wing fanned and, therefore, did not take flight. Females also were capable of flight when disturbed during the daylight hours in Germany where the maximal temperature was high (27–30°C), but not in Siberia, where temperatures peaked at only 17–19°C. However, Siberian females were able to propel themselves off the tree on which they were perched by executing several vigorous wing flicks when approached by the predaceous tettigoniid, Tettigonia caudata.     

THE GENETIC BASIS OF THE TRADE-OFF BETWEEN CALLING AND WING MORPH IN MALES OF THE CRICKET GRYLLUS FIRMUS

Wing dimorphisms exist in a wide range of insects. In wing-dimorphic species one morph is winged has functional flight muscles (LW), and is flight-capable, whereas the other has reduced wings (SW) and cannot fly The evolution and maintenance of wing dimorphisms is believed to be due to trade-offs between flight capability and fitness-related traits. Although there are well-established phenotypic trade-offs associated with wing dimorphism in female insects, there only exist two studies that have established a genetic basis to these trade-offs. The present study provides the first evidence for a genetically based trade-off in male insects, specifically in the sand cricket Gryllus firmus. Because they have to expend energy to maintain the flight apparatus (especially flight muscles), LW males are predicted to call less and therefore to attract fewer females. To be of evolutionary significance, call duration wing morph, and wing muscle condition (size and functionality) should all have measurable heritabilities and all be genetically correlated. Differences between morphs in male G. firmus in the likelihood of attracting a female were tested in the laboratory using a T-maze where females chose between a LW male and a SW male. Call duration for each male was recorded on the sixth day of adult life. A significant difference in call duration was found between SW and LW males (SW = 0.86 ± 0.01, LW = 0.64 ± 0.01 h). SW males attracted significantly more females than did LW males (63% vs. to 37%). All the traits involved in the trade-off had significant heritabilities (call = 0 75 ± 0 33; wing morph = 0.22 ± 007; muscle weight = 0.38 ± 0.09) and genetic correlations (call and wing morph = -0.46 ± 0.20 for SW, -0.68 ± 0.16 for LW; LW call and muscle weight = -0.80 ± 0.14). These results provide the first documented evidence that trade-offs between a dimorphic trait and a fitness-related character in males has a genetic basis and hence can be of evolutionary significance.     

Juvenile hormone as a mediator of plasticity in insect life histories

Insects display much variation in life histories mediated by juvenile hormone. We focus on the contribution of JH to variations in migratory life histories. In many migrants such as the large milkweed bug and the monarch butterfly, JH directly influences migratory flight and the relation between flight and reproduction (oogenesis-flight syndrome). In the true armyworm, JH regulates interactions among female calling, pheromone production, ovarian development, and migration with varying blends of structurally related forms of JH and JH acid. A role for JH also occurs in wing polymorphisms. Aphids regulate wing production via JH-mediated maternal effects; and in crickets, JH esterase modulates the JH influence on wing form. In addition, JH is implicated in wing muscle histolysis. The comprehensive Fairbairn model for JH regulation of wing polymorphisms in flight behavior predicts that JH action will depend on the mode of genetic control, whether single locus or polygenic. Our own studies of the soapberry bug, Jadera haematoloma, reveal a four-morph wing polymorphism in a species rapidly evolving on a new host plant. There are long- and short-winged forms, and the long-winged form displays three degrees of flight muscle histolysis. The polymorphism is subject to both genetic and environmental variations that are mediated by JH. Application of methoprene increases the frequency of the short-winged forms, but there is both within- and between-population genetic variation and genotype by environment interaction (plasticity) in the response to JH. Arch. Insect Biochem. Physiol. 35:359–373, 1997. © 1997 Wiley-Liss, Inc.     

Hybrids of Aphanius dispar and Aphanius mento (Cyprinodontidae: Pisces)

The results of reciprocal hybridization of Aphanius mento and Aphanius dispar are reported. The offspring were examined individually and compared with the parents. It was found that the female hybrids are closer to A. dispar , while the males are closer to A. mento.     

Flight muscles polymorphism in a flightless bug, Pyrrhocoris apterus (L.): developmental pattern, biochemical profile and endocrine control

The flightless bug Pyrrhocoris apterus (L.) is polymorphic for both wing length and flight muscle development. The developed flight muscles of macropterous adults of both sexes first enlarge their volume during the first 5 days after adult emergence, but are then histolyzed in all males and females older than 10 and 14 days, respectively. The flight muscles of brachypterous adult males and females are underdeveloped due to their arrested growth. The total protein content of histolyzed dorsolongitudinal flight muscles from 21-day-old macropterous adults of both sexes is lower than that of developed dorsolongitudinal flight muscles in 5-10-days-old macropterous bugs, but substantially higher than the protein content of underdeveloped dorsolongitudinal flight muscles from adult brachypters. Histolyzed dorsolongitudinal flight muscles differ from the developed ones by decreased quantities of 18 electrophoretically separated proteins. Histolysis of developed dorsolongitudinal flight muscles is accompanied by significant decreases in citrate synthase, glyceraldehyde-3-phosphate dehydrogenase and β-hydroxyacyl-CoA dehydrogenase enzyme activities and an increase in alanine aminotransferase activity, and can be precociously induced by application of a juvenile hormone analogue. This is the first report of flight muscle polymorphism, histolysis of developed flight muscles and its endocrine control in insects displaying non-functional wing polymorphism.     

Transmission-Ratio Distortion through F(1) Females at Chromosome 11 Loci Linked to Om in the Mouse Ddk Syndrome

We determined the genotypes of >200 offspring that are survivors of matings between female reciprocal F(1) hybrids (between the DDK and C57BL/6J inbred mouse strains) and C57BL/6J males at markers linked to the Ovum mutant (Om) locus on chromosome 11. In contrast to the expectations of our previous genetic model to explain the ``DDK syndrome,' the genotypes of these offspring do not reflect preferential survival of individuals that receive C57BL/6J alleles from the F(1) females in the region of chromosome 11 to which the Om locus has been mapped. In fact, we observe significant transmission-ratio distortion in favor of DDK alleles in this region. These results are also in contrast to the expectations of Wakasugi's genetic model for the inheritance of Om, in which he proposed equal transmission of DDK and non-DDK alleles from F(1) females. We propose that the results of these experiments may be explained by reduced expression of the maternal DDK Om allele or expression of the maternal DDK Om allele in only a portion of the ova of F(1) females.     

The trade‐off to macroptery in the cricket Gryllus firmus: a path analysis in males

Among the Orthoptera, wing dimorphism, where one morph is long‐winged and flight capable while the other is short‐winged and flight incapable, is common and believed to be maintained in populations due to trade‐offs to flight capability. In males, macropterous individuals call less than micropterous individuals and as a consequence obtain fewer matings. This trade‐off is hypothesized to be mediated by the energetic costs of calling. In this paper we report results for a path analysis examining lipid weight and DLM (dorso longitudinal muscle) condition of male Gryllus firmus. We found that as DLM condition changes from a nonfunctional to a functional state, call duration decreases, and as lipid weight increases, call duration increases. The most important linked path was wing morph → DLM condition → call duration. This model is consistent with the prediction that the trade‐off between wing morph and call duration is mediated via DLM and lipid stores.     

Trade‐off between flight capability and reproduction in Acridoidea (Insecta: Orthoptera)

In many insect taxa, there is a well‐established trade‐off between flight capability and reproduction. The wing types of Acridoidea exhibit extremely variability from full length to complete loss in many groups, thus, provide a good model for studying the trade‐off between flight and reproduction. In this study, we completed the sampling of 63 Acridoidea species, measured the body length, wing length, body weight, flight muscle weight, testis and ovary weight, and the relative wing length (RWL), relative flight muscle weight (RFW), and gonadosomatic index (GSI) of different species were statistically analyzed. The results showed that there were significant differences in RWL, RFW, and GSI among Acridoidea species with different wing types. RFW of long‐winged species was significantly higher than that of short‐winged and wingless species (p < .01), while GSI of wingless species was higher than that of long‐winged and short‐winged species. The RWL and RFW had a strong positive correlation in species with different wing types (correlation coefficient r = .8344 for male and .7269 for female, and p < .05), while RFW was strong negatively correlated with GSI (r = −.2649 for male and −.5024 for female, and p < .05). For Acridoidea species with wing dimorphism, males with relatively long wings had higher RFW than that of females with relatively short wings, while females had higher GSI. Phylogenetic comparative analysis showed that RWL, RFW, and GSI all had phylogenetic signals and phylogenetic dependence. These results revealed that long‐winged individuals are flight capable at the expense of reproduction, while short‐winged and wingless individuals cannot fly, but has greater reproductive output. The results support the trade‐off between flight and reproduction in Acridoidea.     

Maintenance of variation in sexually selected traits in females: a case study using intrasexual aggression in tree swallows Tachycineta bicolor

A fundamental question in evolutionary biology is how phenotypic variation is maintained in the face of selection that ought to deplete that variation. Much research has investigated this question in traits favored via sexual selection in males, with a common solution implicating the condition dependence of sexually selected phenotypes. Despite growing interest in sexual selection on females, it is not clear if the same mechanisms maintain variation in female ornaments, weaponry or other female behaviors targeted by sexual selection. An important step in testing condition dependence in females is thus to identify whether sexually selected female phenotypes are associated with condition and also with potential costs. Here, I examine these two components of condition dependence for a sexually selected behavior, intrasexual aggression, in female tree swallows Tachycineta bicolor. I asked whether high levels of intrasexual aggression map onto natural variation in female condition and whether aggression is associated with one potential behavioral cost: performance in a vertically challenging test of flight. More aggressive females were heavier for their body size, heavier for their wing size and showed decreased flight ability, relative to less aggressive females. These findings are consistent with condition dependence, where only females in better condition are able to be highly aggressive. The association between high aggression and reduced flight ability may result from the additional lift required to power these relatively heavier birds. These associations between natural variation in aggressive behavior, morphology and flight ability are consistent with condition dependence because they confirm two basic assumptions of condition dependence: a link between aggression and condition, and a link between aggression and a behavioral cost, the speed of escape flight. As the first study to examine these assumptions for a conspicuous behavior favored by intrasexual selection in females, this study suggests broad relevance of condition dependence.     

Physiological trade‐offs between flight muscle and reproductive development in the wing‐dimorphic cricket Velarifictorus ornatus

Morphology, flight muscles, and reproductive development were compared between long‐winged (LW) and short‐winged (SW) morphs of the cricket Velarifictorus ornatus (Shiraki) (Orthoptera: Gryllidae). There was no difference in body weight and pre‐oviposition between the two morphs, but LW individuals had better‐developed flight muscles than SW individuals during and after emergence of the adult. The flight muscles at adult emergence represented 11.9% of the total body weight in the LW female and 4.9% in the SW female. In addition, the weight of the flight muscle of LW females increased by 50% during the first 5 days, whereas the flight muscle of the SW variant increased only slightly after adult emergence. The process of oviposition in LW, SW, and de‐alated females varied: SW females produced more eggs at the early stage than LW females, but de‐alation could shorten the time until the peak of egg laying and caused histolysis of flight muscles of LW females. There was no significant difference in total egg production between the above three groups. In the male, unlike the female, the accessory glands of the two wing morphs enlarged continuously at the same rate. There was no difference between the two wing morphs in the mass of the testes during the first 7 days after adult emergence.     

Fertility in first-generation hybrids of roach, Rutilus rutilus (L.), and silver bream, Blicca bjoerkna (L.)

Fertility in first‐generation hybrids of roach, Rutilus rutilus, and silver bream, Blicca bjoerkna, was investigated. Sperm and egg production of hybrids at first sexual maturity were examined. Eggs from female hybrids were artificially fertilized with the sperm of a corresponding hybrid male; a hybrid male from the reciprocal crossbreeding; a parental species male R. rutilus; and a parental species male B. bjoerkna. The results revealed that gametogenesis was normal in female hybrids. However, in male hybrids, a low efficiency of gametogenesis was observed. The semen of male hybrids was extremely dilute, with spermatozoa concentration lower than that in parental species. Nevertheless, these F1 hybrids (males and females) from reciprocal crossbreeding were fertile. F2 and backcross generations were produced, but F2 crosses from the female hybrid and corresponding hybrid male displayed a drastically slower hatching rate. Also higher proportions of deformed embryos were hatched than in other post‐F1‐generation crosses.     

Inference of adult female dispersal from the distribution of gypsy moth egg masses in a Japanese city

1 The native range of the gypsy moth Lymantria dispar (L.) spans the temperate forests of Eurasia. Across this region, a clinal female flight polymorphism exists; gypsy moth females in eastern Asia are mostly capable of directed flight, those in western and southern Europe are largely incapable of flight and populations distributed across the centre of the distribution exhibit a range of intermediate flight behaviours. 2 Although information exists about the timing and duration of female flight from laboratory and wind tunnel studies, little or no quantitative data are available on average distances flown by Asian gypsy moth females prior to oviposition in the field. This information is critical for estimating risk of contamination at specific ports and transit terminals, as well as for predicting the spread of populations that might someday invade currently uninfested regions of the world. 3 In the present study, an extensive visual survey of gypsy moth egg masses was conducted during a walk through streets and paths in a 3.92 × 5.76 km area in Kanazawa, Japan. This area consisted of a matrix of urban, agricultural and forest land uses. The distribution of egg masses relative to distances from host forests was used to infer the magnitude of pre‐ovipositional female flight. 4 A total of 3172 egg masses was recorded from surveys conducted during the search of a path totalling 384 km. Within urban areas, egg masses were most abundant in the area <1 km from the edge of forest land. 5 These results suggest that most female gypsy moth flight is limited to the area within 1 km of host forests. They also suggest that shipping containers and other parcels located >1 km from forests are at a much lower risk of contamination with Asian gypsy moth egg masses.     

Paternal inheritance of egg traits in mice: a case of genomic imprinting

Eggs from reciprocal hybrids between the C57BL/6By and BALB/cBy strains were tested for their susceptibility to attack by hyaluronidase and pronase. There were significant reciprocal differences between the F1 females in the responses of their unfertilized eggs to both enzymes. The F1 hybrids from BALB mothers showed the increased susceptibility characteristic of C57BL whilst the F1 hybrids with C57BL mothers were more resistant to both enzymes, like BALB mice. Eggs from the four kinds of reciprocal F2 hybrid females also showed patroclinous patterns of susceptibility. A patroclinous difference was found between reciprocal crosses of the CXBD and CXBE recombinant inbred strains but not in crosses between recombinant inbred strains with similar phenotypes. Cross fostering did not alter the phenotypes of the C57BL and BALB females or those of their reciprocal F1 hybrids. The findings are interpreted in terms of differential genomic imprinting of paternally inherited information. The possible general usefulness of patroclinous differences between reciprocal F1 females in revealing differences in imprinting is noted.     

Impaired flight ability during incubation in the pied flycatcher

During the breeding season, many female passerine birds increase in body mass before egg laying, maintain a relatively high body mass during incubation, and then drop back to the original level during the chick-rearing period. The post-hatching reduction in body mass, which can be as large as 10–20%, has been suggested to represent an adaptive mass loss to reduce wing loading, thereby increasing parental flight efficiency when chicks have hatched and have to be fed. Here we present the first study of changes in flight ability from incubation to chick rearing in birds. Wild female pied flycatchers Ficedula hypoleuca flew more slowly during incubation than during chick rearing; a 7% reduction in body mass after the chicks had hatched was associated with a 10% increase in vertical take-off speed. Furthermore, the flight muscle size of the females tracked the reduction in wing load, suggesting that muscle size was adaptively reduced when no longer needed. Since incubation-feeding by males reduces the time females have to spend outside the nest foraging, our results suggest that in addition to increasing female nutritional status and reducing incubation time, incubation-feeding will also reduce predation risk during the period when females face impaired flight ability.