Wing Growth Research Articles

Scaling between cell cycle duration and wing growth is regulated by Fat-Dachsous signaling in Drosophila.

The atypical cadherins Fat and Dachsous (Ds) signal through the Hippo pathway to regulate growth of numerous organs, including the Drosophila wing. Here, we find that Ds-Fat signaling tunes a unique feature of cell proliferation found to control the rate of wing growth during the third instar larval phase. The duration of the cell cycle increases in direct proportion to the size of the wing, leading to linear-like growth during the third instar. Ds-Fat signaling enhances the rate at which the cell cycle lengthens with wing size, thus diminishing the rate of wing growth. We show that this results in a complex but stereotyped relative scaling of wing growth with body growth in Drosophila. Finally, we examine the dynamics of Fat and Ds protein distribution in the wing, observing graded distributions that change during growth. However, the significance of these dynamics is unclear since perturbations in expression have negligible impact on wing growth.

Scaling between cell cycle duration and wing growth is regulated by Fat-Dachsous signaling in Drosophila

Scaling between cell cycle duration and wing growth is regulated by Fat-Dachsous signaling in Drosophila

Trait‐specific sensitive developmental windows: Wing growth best integrates weather conditions encountered throughout the development of nestling Alpine swifts

AbstractThe size and growth patterns of nestling birds are key determinants of their survival up to fledging and long‐term fitness. However, because traits such as feathers, skeleton and body mass can follow different developmental trajectories, our understanding of the impact of adverse weather on development requires insights into trait‐specific sensitive developmental windows. We analysed data from nestling Alpine swifts in Switzerland measured throughout growth up to the age of 50 days (i.e. fledging between 50 and 70 days), for wing length and body mass (2693 nestlings in 25 years) and sternum length (2447 nestlings in 22 years). We show that the sensitive developmental windows for wing and sternum length corresponded to the periods of trait‐specific peak growth, which span almost the whole developmental period for wings and the first half for the sternum. Adverse weather conditions during these periods slowed down growth and reduced size. Although nestling body mass at 50 days showed the greatest inter‐individual variation, this was explained by weather in the two days before measurement rather than during peak growth. Interestingly, the relationship between temperature and body mass was not linear, and the initial sharp increase in body mass associated with the increase in temperature was followed by a moderate drop on hot days, likely linked to heat stress. Nestlings experiencing adverse weather conditions during wing growth had lower survival rates up to fledging and fledged at later ages, presumably to compensate for slower wing growth. Overall, our results suggest that measures of feather growth and, to some extent, skeletal growth best capture the consequences of adverse weather conditions throughout the whole development of offspring, while body mass better reflects the short, instantaneous effects of weather conditions on their body reserves (i.e. energy depletion vs. storage in unfavourable vs. favourable conditions).

Impact of Laser Cavity Configurations and Pump Radiation Parameters on the Characteristics of High-Energy Yellow Raman Lasers Based on Potassium Gadolinium Tungstate Crystals

In this paper, the influence of pump radiation parameters and laser resonator configurations on the characteristics of high-energy 589 nm KGW Raman lasers is investigated and explained. The best energy efficiency is obtained in lasers with a flat resonator, while the best angular characteristics are obtained in lasers with an unstable resonator. The use of stable spherical resonators results in the worst energy and angular characteristics. The angular divergence in lasers with flat cavities increases with pump intensity because of wing growth, whereas the core width remains unchanged. The structure of the wings is recorded and analyzed.

Decoupling of body size, physiological state and subsequent performance in a developmentally manipulated songbird

Abstract It is generally assumed that larger juveniles are more physiologically mature, hence their overall condition and subsequent performance are higher. Some taxa face extreme workload transitions during development (e.g. nest departure in birds), which may select for non‐linear growth profiles that decouple relationships between body size and physiological state, making the links between metrics of development (e.g. body mass) and juvenile performance uncertain. We manipulated perceived mass in European starlings approaching fledging using 4.0 g weighted backpacks, measuring subsequent growth trajectories (mass, wing length) and physiological state (aerobic capacity, energy state, oxidative status) to test whether body size and physiology are coupled during a non‐linear developmental phase (pre‐fledging mass recession). Nanotag radio transmitters were then used to track post‐fledging performance (activity, activity‐slope, dispersal). Weighted nestlings had greater pre‐fledging mass recession and marginally reduced wing growth when compared to controls. Consequently, weighted birds had lower body mass at fledging, while also displaying markers of oxidative stress (increased reactive oxygen metabolites), yet aerobic capacity and energy state were equal between treatment groups. Previously weighted birds showed no correlation between fledgling state (body size, physiology) and subsequent performance. However, control fledglings that had decreased mass recession and greater wing growth prior to fledging dispersed earlier, while longer wings at fledging were associated with more rapid increases in post‐fledging activity (activity‐slope). In addition, control fledglings with lower haemoglobin also dispersed earlier, while increased reactive oxygen metabolites were associated with decreased activity levels. Body mass and energy state were unrelated to any metric of post‐fledging performance. Our data suggest mass‐independent development of some physiological traits in species with non‐linear growth profiles, potentially with a context‐dependent oxidative cost, and that physiology may predict some measures of post‐fledging performance not captured by body size. Read the free Plain Language Summary for this article on the Journal blog.

Initiation and evolution of butterflies in roller bearings due to rolling contact fatigue

This investigation entails analysis of 520 butterfly formations (BFs) and non-metallic inclusions without BFs in two RCF-tested roller bearings to elucidate the influence of inclusion characteristics and stress level they are subject to, on the initiation and growth of BFs. The results show duplex inclusions, though least frequent in the bearing steels, exhibit the highest butterfly formation rate comparing with pure sulphide/oxide inclusions. It is also found that larger inclusions and those with smaller aspect ratios are more prone to butterfly formation; BF wing length decreases with the increase of inclusion aspect ratio; BF orientation is significantly influenced by inclusion size and stress level; stress magnitude appears to either impede or facilitate BF wing growth depending on BF orientation.

Allometric wing growth links parental care to pterosaur giantism.

Pterosaurs evolved a broad range of body sizes, from small-bodied early forms with wingspans of mostly 1-2 m to the last-surviving giants with sizes of small airplanes. Since all pterosaurs began life as small hatchlings, giant forms must have attained large adult sizes through new growth strategies, which remain largely unknown. Here we assess wing ontogeny and performance in the giant Pteranodon and the smaller-bodied anurognathids Rhamphorhynchus, Pterodactylus and Sinopterus. We show that most smaller-bodied pterosaurs shared negative allometry or isometry in the proximal elements of the fore- and hindlimbs, which were critical elements for powering both flight and terrestrial locomotion, whereas these show positive allometry in Pteranodon. Such divergent growth allometry typically signals different strategies in the precocial-altricial spectrum, suggesting more altricial development in Pteranodon. Using a biophysical model of powered and gliding flight, we test and reject the hypothesis that an aerodynamically superior wing planform could have enabled Pteranodon to attain its larger body size. We therefore propose that a shift from a plesiomorphic precocial state towards a derived state of enhanced parental care may have relaxed the constraints of small body sizes and allowed the evolution of derived flight anatomies critical for the flying giants.

Is Drosophila Dpp/BMP morphogen spreading required for wing patterning and growth?

Secreted signaling molecules act as morphogens to control patterning and growth in many developing tissues. Since locally produced morphogens spread to form a concentration gradient in the surrounding tissue, spreading is generally thought to be the key step in the non-autonomous actions. Here, we review recent advances in tool development to investigate morphogen function using the role of decapentaplegic (Dpp)/bone morphogenetic protein (BMP)-type ligandin the Drosophila wing disc as an example. By applying protein binder tools to distinguish between the roles of Dpp spreading and local Dpp signaling, we found that Dpp signaling in the source cells is important for wing patterning and growth but Dpp spreading from this source cells is not as strictly required as previously thought. Given recent studies showing unexpected requirements of long-range action of different morphogens, manipulating endogenous morphogen gradients by synthetic protein binder tools could shed more light on how morphogens act in developing tissues.

Crucial DNA at crux of insect wing size evolution

Closely related species are usually remarkably similar. But take a closer look, and subtle differences begin to emerge. Some may have longer limbs or wider bodies, and some fruit fly species have dinky wings while the wings of relatives are relatively large. ‘The diversity of wing size relative to whole body size is remarkable in insects, but it is currently unclear how wing-to-body proportions have changed through evolution’, says Marcos Nahmad from the Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav-IPN), Mexico. The proteins that control the development of wings are essentially the same across almost all fruit fly species, regardless of their physical differences, so how do these differences come about?Regions of DNA that control how the regulatory proteins are produced could tweak the way in which a limb develops. One member of the fruit fly family, Drosophila virilis, has petite wings compared with D. melanogaster and other species, which all have relatively large wings compared with their bodies. Knowing this, Nahmad and Timothy Evans (University of Arkansas, USA) wondered if a region of regulatory DNA found in the gene for a protein known as ‘vestigial’ – which controls wing growth – could be responsible for D. virilis’s smaller wings. If so, could D. melanogaster grow D. virilis-sized wings if Keity Farfán-Pira and Teresa Martinez-Cuevas (from Cinvestav-IPN) replaced the key section of D. melanogaster DNA with regulatory DNA from D. virilis?First, Farfán-Pira confirmed that D. virilis fruit flies develop smaller wings for their body size, and then she began the painstaking task of transferring a 1200 bp segment of D. virilis DNA from the section of DNA preceding the fly's vestigial gene into the correct place in the DNA of D. melanogaster eggs. In addition, the team added a gene that would turn the modified flies’ eyes fluorescent red, to be sure that the offspring produced by the D. melanogaster eggs carried the crucial D. virilis DNA.Eventually, after months of patience in the laboratory creating the genetically modified D. melanogaster eggs and then waiting for them to develop into flies, Farfán-Pira measured the wing and leg lengths of the insects and the team was astonished that the wings of the D. melanogaster carrying D. virilis DNA were far smaller for their body size than those of regular D. melanogaster. ‘We were shocked’, Nahmad admits. Inserting the D. virilis vestigial regulatory DNA sequence into the D. melanogaster vestigial gene was sufficient to make the flies’ wings smaller, like the daintier wings of D. virilis.But what does this discovery mean for how members of the insect family, ranging from flamboyant butterflies to stubby-winged bees, evolved such extensive wing differences given that they all use the same cellular machinery to coordinate wing development? The team suspects that the crucial section of vestigial gene DNA fine-tunes the distribution of the cell signalling proteins that regulate wing growth through the larvae's imaginal disk structure – which develops into the wings – to regulate wing size and allow the insect to develop either small or large wings, depending on their family history. The team concludes that some significant change in the key vestigial DNA segment occurred after the split between the D. melanogaster and D. virilis families, resulting in one branch of the family with relatively large wings while the other evolved their comparatively small wings, which persist to this day.

RNAi screen in the Drosophila wing of genes encoding proteins related to cytoskeleton organization and cell division

Cell division and cytoskeleton organization are fundamental processes participating in the development of Drosophila imaginal discs. In this manuscript we describe the phenotypes in the adult fly wing generated by knockdowns of 85% of Drosophila genes encoding proteins likely related to the regulation of cell division and cytoskeleton organization. We also compile a molecular classification of these proteins into classes that describe their expected or known main biochemical characteristics, as well as mRNA expression in the wing disc and likely protein subcellular localization for a subset of these genes. Finally, we analyze in more detail one protein family of cytoskeleton genes (Arp2/3 complex), and define the consequences of interfering with cell division for wing growth and patterning.

Psi promotes Drosophila wing growth via direct transcriptional activation of cell cycle targets and repression of growth inhibitors.

The first characterised FUSE Binding Protein family member, FUBP1, binds single-stranded DNA to activate MYC transcription. Psi, the sole FUBP protein in Drosophila, binds RNA to regulate P-element and mRNA splicing. Our previous work revealed pro-growth functions for Psi, which depend, in part, on transcriptional activation of Myc. Genome-wide functions for FUBP family proteins in transcriptional control remain obscure. Here, through the first genome-wide binding and expression profiles obtained for a FUBP family protein, we demonstrate that, in addition to being required to activate Myc to promote cell growth, Psi also directly binds and activates stg to couple growth and cell division. Thus, Psi knockdown results in reduced cell division in the wing imaginal disc. In addition to activating these pro-proliferative targets, Psi directly represses transcription of the growth inhibitor tolkin (tok, a metallopeptidase implicated in TGFβ signalling). We further demonstrate tok overexpression inhibits proliferation, while tok loss of function increases mitosis alone and suppresses impaired cell division caused by Psi knockdown. Thus, Psi orchestrates growth through concurrent transcriptional activation of the pro-proliferative genes Myc and stg, in combination with repression of the growth inhibitor tok.

Moult intensity constraints along the complete moult sequence of the House Sparrow (Passer domesticus)

Sequence and intensity are two essential components of bird moult. While the moult sequences of remex tracts are highly homogenous across passerines, other tracts apparently show a high variability. Moreover, order of moult activation among tracts are insufficiently known. Likewise, dynamics of moult intensity as moult progresses remains poorly known. Here, we provide detailed quantitative description of moult sequence and intensity in the House Sparrow (Passer domesticus). To understand their role, we tested two hypotheses on the: 1) protection function of moult sequence, and 2) aerodynamic and physiological constraints on moult intensity. We scored percentage growth of 313 captured sparrows using the mass of the feathers of each tract (also length for remiges) to monitor moult intensity throughout the complete moult progress, which is defined as the fraction of new and growing feathers in a moulting bird relative to the total plumage. Moult sequence was highly variable both within wing coverts and among feather tracts, with moult sequence differing among all birds to some degree. We only found support for the protection function between greater coverts and both tertials and secondaries. Remex-moult intensity conformed to theoretical predictions, therefore lending support to the aerodynamic-constraint hypothesis. Furthermore, remex-moult speed plateaued during the central stages of moult progress. However, overall plumage-moult speed did not fit predictions of the physiological-constraint hypothesis, showing that the remex moult is only constrained by aerodynamics. Our results indicate that aerodynamic loss is not simply the inevitable effect of moult, but that moult is finely regulated to reduce aerodynamic loss. We propose that the moult of the House Sparrow is controlled through sequence and intensity adjustments in order to: 1) avoid body and wing growth peaks; 2) fulfil the protection function between some key feather tracts; 3) reduce detrimental effects on flight ability; 4) keep remex sequence fixed; and 5) relax remex replacement to last the whole moult duration.

Mitochondria dysfunction impairs Tribolium castaneum wing development during metamorphosis

The disproportionate growth of insect appendages such as facultative growth of wings and exaggeration of beetle horns are examples of phenotypic plasticity. Insect metamorphosis is the critical stage for development of pupal and adult structures and degeneration of the larval cells. How the disproportionate growth of external appendages is regulated during tissue remodeling remains unanswered. Tribolium castaneum is used as a model to study the function of mitochondria in metamorphosis. Mitochondrial dysfunction is achieved by the knockdown of key mitochondrial regulators. Here we show that mitochondrial function is not required for metamorphosis except that severe mitochondrial dysfunction blocks ecdysis. Surprisingly, various abnormal wing growth, including short and wingless phenotypes, are induced after knocking down mitochondrial regulators. Mitochondrial activity is regulated by IIS (insulin/insulin-like growth factor signaling)/FOXO (forkhead box, sub-group O) pathway through TFAM (transcription factor A, mitochondrial). RNA sequencing and differential gene expression analysis show that wing-patterning and insect hormone response genes are downregulated, while programmed cell death and immune response genes are upregulated in insect wing discs with mitochondrial dysfunction. These studies reveal that mitochondria play critical roles in regulating insect wing growth by targeting wing development during metamorphosis, thus showing a novel molecular mechanism underlying developmental plasticity.

Analysis of the Drosophila Ajuba LIM protein defines functions for distinct LIM domains.

The Ajuba LIM protein Jub mediates regulation of Hippo signaling by cytoskeletal tension through interaction with the kinase Warts and participates in feedback regulation of junctional tension through regulation of the cytohesin Steppke. To investigate how Jub interacts with and regulates its distinct partners, we investigated the ability of Jub proteins missing different combinations of its three LIM domains to rescue jub phenotypes and to interact with α-catenin, Warts and Steppke. Multiple regions of Jub contribute to its ability to bind α-catenin and to localize to adherens junctions in Drosophila wing imaginal discs. Co-immunoprecipitation experiments in cultured cells identified a specific requirement for LIM2 for binding to Warts. However, in vivo, both LIM1 and LIM2, but not LIM3, were required for regulation of wing growth, Yorkie activity, and Warts localization. Conversely, LIM2 and LIM3, but not LIM1, were required for regulation of cell shape and Steppke localization in vivo, and for maximal Steppke binding in co-immunoprecipitation experiments. These observations identify distinct functions for the different LIM domains of Jub.

Requirement of Myoglianin for metamorphosis in the beetle Henosepilachna vigintioctopunctata.

Henosepilachna vigintioctopunctata is a serious defoliating beetle attacking Solanaceae and Cucurbitaceae plants in many Asian countries. In the present paper, we identified a putative myoglianin (myo) gene. Hvmyo was actively transcribed throughout development, from embryo to adult. RNA interference (RNAi)-aided knockdown of Hvmyo delayed larval development by more than 2 days, reduced larval body size, inhibited the growth of antennae, wings and legs and disturbed gut purge. Knockdown of Hvmyo impaired the larval-pupal transition. All the Hvmyo RNAi larvae arrested at the larval stage or formed misshapen pupae or adults. The deformed pupae and adults were partially wrapped with exuviae, bearing separated wings. Moreover, the expression levels of five ecdysteroidogenesis genes (Hvspo, Hvphm, Hvdib, Hvsad and Hvshd), a prothocicotropic hormone (PTTH)/Torso pathway gene (Hvtorso), two 20E receptor genes (HvEcR and HvUSP), and two 20E signalling genes (HvE93 and HvFTZ-F1) were as a result of HvMyo RNAi significantly lowered. Conversely, the expression of a JH biosynthesis gene (Hvjhamt), a JH receptor gene HvMet and a JH signalling gene HvKr-h1 was greatly enhanced. Although ingestion of 20E and Hal rescued the 20E signal, it could not alleviate larval performance and defective phenotypes. Our results suggest that Myo exerts four distinctive roles in ecdysteroidogenesis, JH production, organ growth and larva-pupa-adult transformation in H. vigintioctopunctata.

Broad complex and wing development in cockroaches

In hemimetabolan insects, the transcription factor Broad complex (Br–C) promotes wing growth and development during the nymphal period. We wondered whether Br–C could trigger the initiation of wing development, using the cockroach Blattella germanica as a model. We show that first instar nymphs have their unique identity of these three thoracic segments specified. During embryogenesis, the expression of Br–C and some wing-related genes show two matching waves. The first takes place before the formation of the germ band, which might be involved in the establishment of various developmental fields including a potential “wing field”, and the second wave around organogenesis, possibly involved in the initiation of wing development. However, the expression of Br–C in early embryogenesis concentrates in the developing central nervous system, thus not co-localizing with the expression of the typical wing-related gene vestigial, which is expressed at the edge of the thoracic and abdominal segments. This suggests that Br–C is not specifically involved in the establishment of a potential “wing field” in early embryogenesis. Moreover, maternal RNAi for Br–C depletes the first wave of Br–C expression but does not affect the early expression of wing-related genes. As maternal Br–C RNAi did not deplete the second expression wave of Br–C, we could not evaluate if Br–C is involved in the initiation of wing development. Alternatively, using nymphal RNAi of Br–C and Sex combs reduced (Scr), we show that Br–C contributes to the formation of ectopic wing structures that develop in the prothorax when Scr is depleted. The gene most clearly influenced by Br–C RNAi is nubbin (nub), which, in nymphs is crucial for wing growth. Together, these results suggest that Br–C does not specifically contribute to the establishment of the “wing field”, but it does seem important later, in the initiation of wing development, enhancing the expression of wing-related genes, especially nub. This supports the hypothesis previously proposed by the authors, whereby Br–C might have facilitated the evolution of holometaboly. However, there is no doubt that other factors have also contributed to this evolution.

Flexible growth and body mass predict physiological condition at fledging in the synchronously breeding European starling, Sturnus vulgaris.

Recent studies have reported beneficial carryover effects of juvenile development that predict interspecific survival differences at independence. Yet, traits relating to body size (i.e. morphological traits) have proven to be unreliable predictors of juvenile survival within species. Exploring individual variation of growth trajectories and how they covary with physiology could reveal species-specific developmental modes which have implications for our assessments of juvenile quality. Here, we investigated morphological development of European starlings (Sturnus vulgaris) approaching fledging in relation to three components of physiological condition at independence: aerobic capacity, energy state and oxidative status. We found evidence of flexible mass and wing growth which independently covaried with fledgling energy state and aerobic capacity, respectively. By comparison, tarsus and wing length at fledging were unrelated to any physiological trait, while mass was positively associated with principal component scores that comprised aerobic capacity and energy state. Thus, flexible growth trajectories were consistent with ‘developmental plasticity’: adaptive pre-fledging mass recession and compensatory wing growth, which seemingly came at a physiological cost, while fledgling body mass positively reflected overall physiological condition. This highlights how patterns of growth and absolute size may differently reflect fledgling physiology, potentially leading to variable relationships between morphological traits and juvenile fitness.

A hemimetabolous wing development suggests the wing origin from lateral tergum of a wingless ancestor

The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion. The mechanism of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand where and how insect wings evolutionarily originate. This study explored the developmental origin and the postembryonic dramatic growth of wings in the cricket Gryllus bimaculatus. We find that the lateral tergal margin, which is homologous between apterygote and pterygote insects, comprises a growth organizer to expand the body wall to form adult wing blades in Gryllus. We also find that Wnt, Fat-Dachsous, and Hippo pathways are involved in the disproportional growth of Gryllus wings. These data provide insights into where and how insect wings originate. Wings evolved from the pre-existing lateral terga of a wingless insect ancestor, and the reactivation or redeployment of Wnt/Fat-Dachsous/Hippo-mediated feed-forward circuit might have expanded the lateral terga.

Variation in growth patterns of Marsh Harrier Circus aeruginosus nestlings: effects of hatching order, nestling subperiod, brood size and weather conditions

Post-natal growth has long-term consequences for survival and fitness in birds and is subject to strong directional selection. Highly variable patterns of nestling development are influenced by an array of extrinsic and intrinsic factors. This study analysed the impacts of hatching order, nestling subperiod, brood size and weather conditions, all of which could influence the growth rate of Marsh Harrier Circus aeruginosus nestlings. It was conducted over a period of 6 years, during which measurements of 173 nestlings from 66 nests were made at fishpond complexes in eastern Poland. Relative growth rates (RGR) were calculated on the basis of tarsus and wing lengths during two subperiods of nestling development. Linear mixed models showed that the hatching order and nestling subperiod influenced nestling growth, whereas brood size did not affect wing or tarsus relative growth rates. The effect of hatching order differed between the two traits and between subperiods. Marginal nestlings in broods of five exhibited poor wing growth and perished before fledging. In contrast to wing growth, tarsus growth rates were similar in all the siblings in the first subperiod. During the second developmental subperiod, the growth rates of both locomotor traits exhibited the same pattern, i.e., higher values in the later-hatched chicks than in the earlier ones. Precipitation, but not temperature, had a negative impact on growth in the second subperiod. Our results show a variation in growth patterns between nestmates, which was the most evident in the rate of wing growth. The study enhances our understanding of brood reduction and cainism in birds of prey.

Forest logging is associated with shape of males and gynes in the wood ant Formica aquilonia

Environmental stress can affect individual development and fitness in insects. Forest logging is a serious environmental stress for forest-specialist insects, such as the mound-building wood ant Formica aquilonia Yarrow 1955, which builds its nests into forests and is dependent on the nutrition provided by the forest habitat. We studied whether the logging causes such a strong environmental stress that it would be visible in disproportionate growth and shape of young winged wood ant gynes (‘queens’) and males. We measured head width, thorax width and wing length of 144 gynes and 100 males from 12 nests from six clear-cut areas, 11 nests from unlogged forest stands and 10 nests in clear-cut—forest margins. We observed disproportionate growth of different body parts and allometric growth of wings in both sexes in areas with different logging-induced disturbance. Gynes had larger heads in clear-cut areas and males had narrowest thoraxes in forest clear-cut edges. With an increasing thorax width, the wing length decreases steeper in clear-cuts than in other habitats in gynes and increases steeper in clear-cuts than other habitats in males. It seems that in a strongly disturbed clear-cut environment, the gynes invest the growth of head width. There seems to be a trade-off between the growth of the thorax and wings in gynes but not in males. The altered body shape may be adaptation to clearings caused by storm events of wild fires, but not forest management practices of modern era. Large-headed gynes may be better in a colony take-over, needed for the establishment of new colonies in early succession stage habitats in this temporally social parasitic species. Long-winged males may have better long-range flight ability, and they may thus have better fitness and change to disperse their genes onto new habitats.