Flightless Females Research Articles

Exploring the Effects of Plant Odors, from Tree Species of Differing Host Quality, on the Response of Lymantria disparMales to Female Sex Pheromones.

A widely accepted hypothesis for host-plant selection in herbivorous insects is that ovipositing females select host-plants that maximize the survival and performance of their offspring. However, numerous studies indicate that this is not always the case for polyphagous species. Lymantria dispar is a highly polyphagous forest defoliator and has flightless females in some subspecies, resulting in a limited capacity to make host-choices. Males of other Lepidopteran species utilize a combination of sexual pheromones and plant volatiles in their mating choices and exhibit preferences among plant species. We explored the behavior of L. dispar males towards sexual pheromone in the presence and absence of plant volatiles and their ability to discriminate between two plant species with different degrees of suitability for their offspring: a suboptimal host (Pinus sylvestris), and an optimal host (Quercus robur). In no-choice wind tunnel assays, we found that rates of male success in locating a pheromone source were not altered by the presence of plant odors; however, the time spent by males searching for the pheromone source after reaching the full length of the tunnel was reduced by more than 50% in the presence of plant volatiles. In dual choice assays, males exhibited a clear preference for a combination of pheromones and plant volatiles over the pheromone alone. However, we did not find evidence of an innate ability to discriminate between the odors of optimal and suboptimal host plants. We discuss possible ecological and evolutionary explanations for these observations.

Sex-biased response in activity to light sources with different spectral composition in geometrid moths with flightless females (Lepidoptera: Geometridae)

Geometrid moths occurring in late autumn and early spring in temperate forest habitats are often harmful defoliators of deciduous stands. Their populations can cause locally cyclic outbreaks and thus preventive monitoring actions have been developed, mainly based on pheromone attraction of males. Females are mostly flightless with reduced or lost wings and reduced senses associated with flying. Males are standard flyers with well-developed eyes and must be able to deal with rapidly changing light conditions during their activity. Although such differences indicate sex-biased differences in reactions to light, this has been insufficiently tested. In conditions of an experimental arena and using light-emitting diodes, we tested the different reactions of the sexes for nine species to precisely defined short segments of the electromagnetic spectrum in the range 360-660 nm. Across all species, males preferred shorter wavelengths up to 500 nm, while females were nonselective and generally less active. The sexes differed by eye size and body mass, with males having significantly larger eyes and lower body mass. Between brachypterous and apterous females, the former had larger eye size, while body mass differences were statistically insignificant. There were differences between the sexes in move-to-light reactions and changes in eye size and body mass in line with wing reduction. While males preferred a relatively distinct range of shorter wavelengths, a method of attraction to lights with distinct narrow spectra could be used markedly to enhance the established methods of forest pest monitoring, either alone or in combination with chemical male attraction.

Forest edges enhance mate‐finding in the invasive European gypsy moth, Lymantria dispar

AbstractHabitat type, fragmentation, and edge effects can play important roles in the mate‐finding abilities of many species. These effects can be particularly pronounced in low‐density populations, which are often found at the margins of species' ranges or at the leading edge of an invasion. The European gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae), is a non‐native insect defoliator in the USA and Canada, where flightless females attract male moths through pheromone production and local extirpation of low‐density populations can be due to mate‐finding failure. To assess the effects of habitat edges on the ability of gypsy moths to find mates, we conducted a release experiment with male gypsy moths using female‐baited trap arrays in fields, at forest edges, and in the forest interior. Reduced mate‐finding was expected in fields and near forest edges based on geographic variation in invasion rates, male flight behavior, and pheromone plume dynamics. However, we found that mate‐finding was highest at forest edges, reduced in fields, and lowest within the forest interior. Within an array, traps closest to the forest edge also had the highest mate‐finding, suggesting that habitat characteristics can influence male flight direction in addition to pheromone cues. These results suggest that a moderate level of forest fragmentation enhances mate‐finding ability in the gypsy moth. Understanding the relationship between habitat heterogeneity and mate‐finding success in invasive species can inform predictions of future spread and assist with management plans that target mating disruption.

Evolutionary history of Apocheima cinerarius (Lepidoptera: Geometridae), a female flightless moth in northern China

The alterations in the phylogeographical structures of insects in response to the uplift of the Qinghai–Tibet Plateau and the Quaternary glaciations in eastern Asia, particularly in northern China, remain largely unknown. In this study, we selected Apocheima cinerarius, a moth with flightless females, using molecular data (complete mitochondrial genomes and nuclear data) and ecological niche modelling (ENM) to investigate the effects of paleoclimatic changes on the evolutionary history of insects in the area of northern China. The phylogenetic tree of complete mitochondrial genomes indicated that there were two lineages, the western and eastern lineages. The nuclear gene analyses also detected unique haplotypes in each lineage. Time of the most recent common ancestor (TMRCA) of the two lineages was approximately in Early–Middle Pleistocene. Bayesian skyline plots revealed that the western lineage underwent a population expansion event after the Last Glacial Maximum, whereas the eastern lineage underwent expansion between the Last Interglacial and the Last Glacial Maximum. Our results suggest that A. cinerarius expanded eastward from western sites until the moth was distributed across the entire region of northern China. Then, A. cinerarius underwent contraction into isolated glacial refugia followed by subsequent expansion driven by Pleistocene climate changes, which established a narrow sympatric area. Our results indicate that the Quaternary environmental fluctuations had profound influences on the diversification and demography of an insect in northern China, and the same species in north‐western China and north‐eastern China have different demographic histories.

The Males of Rhynchomicropteron (Diptera: Phoridae)

The genus Rhynchomicropteron Annandal (1912) has distinctive, myrmecophilous, flightless females. The females of the 17 Oriental species are keyed by Disney & Kistner (1998), supplemented by Disney (1999, 2010). Until Brown (1992) reared R. nudiventer Papp in Thailand, the males had been assigned to the genus Gymnoselia Schmitz (1927). This ‘genus’ contained the type species, R. curvescens (Schmitz 1927) and R. nudicosta (Brues 1907). Neither of these have been linked to their females. Recently Lengyel (2011) has described both sexes of a species from Israel, and reported the presence of this genus in Africa and Australia. The males remain poorly known. The purpose of this paper is to provide a key to the known males, even though most remain unknown and some are given code numbers only until they can be linked to their females.

Sexual dimorphism, mating systems, and nuptial gifts in two Asian fireflies (Coleoptera: Lampyridae)

Many insect taxa show conspicuous sexual dimorphism in which females lack functional wings and are therefore incapable of flight. In fireflies, this loss of female flight is correlated with male production of spermatophore nuptial gifts, with species with flightless females also lacking gift production. In this study we further examined the relationship between sexual dimorphism and nuptial gifts by examining the reproductive ecology of two Asian fireflies, the sexually monomorphic Aquatica ficta (Luciolinae) and dimorphic Pyrocoelia pectoralis (Lampyrinae). We describe the reproductive anatomy of P. pectoralis males and females, and the time course of A. ficta spermatophore transfer. Through a series of mating experiments, we determined the effect of the number of matings on female fecundity, egg hatching success and female lifespan. The spermatophore-producing A. ficta was found to be monandrous, and female lifespan doubled as a result of that single mating. P. pectoralis was found to lack spermatophores but females were polyandrous and fecundity and egg hatching success both increased with additional matings. These results contradict patterns known from North American firefly species and provide insight into the role of male-derived substances in mating systems.

Emeia gen. nov., a new genus of Luciolinae fireflies from China (Coleoptera: Lampyridae) with an unusual trilobite-like larva, and a redescription of the genus Curtos Motschulsky

Emeia, a new genus of Luciolinae fireflies, is described from males, flightless females and unusual trilobite-like larvaefor a single species pseudosauteri (Geisthardt) transferred from Curtos Motschulsky. Flashing patterns and ecological dataare presented. A phylogenetic analysis covering 143 Luciolinae species uses 436 morphological characters of males, fe-males and larvae to support the erection of the new genus. A generic redescription of Curtos Motschulsky from a restricted number of species is given. A key to genera and certain species groups using males is provided.

Generic placement of the Neotropical species of “Phragmatobia” (Erebidae, Arctiinae), with a remarkable matrivorous species from the Peruvian Andes

Phragmatobia Stephens is briefly reviewed and a diagnosis is provided. The South American species currently placed in Phragmatobia Stephens are revised to two new genera, Andesobia Schmidt and De Freina, gen. n., and Patagobia Schmidt and De Freina, gen. n. (subtribe Spilosomina). Both Andesobia and Patagobia exhibit adaptations to high altitude habitats, including micropterous females in Andesobia (Patagobia females are unknown) and diurnal flight of males. The adults, immature stages, and mating behaviour of Andesobia jelskii (Oberthür, 1881) are described. Males of Andesobia jelskii enter the female cocoon to mate, and the micropterous, flightless females remain in the cocoon following oviposition where newly hatched larvae feed initially on the female’s body.Four species are included in Andesobia, Andesobia jelskii comb. n. (= Paracles imitatrix Rothschild, 1922, syn. n.), Andesobia flavata (Hampson, 1901), comb. n., Andesobia boliviana (Gaede, 1923), comb. n. (=Turuptiana flavescens Rothschild, 1933, syn. n.), and Andesobia sanguinea (Hampson, 1907), comb. n. Patagobia includes only Patagobia thursbyi (Rothschild, 1910), comb. n., and Patagobia thursbyi pluto Toulgoët is relegated to its synonymy. Patagobia shows affinities to Phaos Walker, 1855 of Australia, Metacrias Meyrick, 1886 of New Zealand, and Pseudophragmatobia Krüger, 2009 of South Africa, suggesting a common ancestry of circumantarctic origin. Phragmatobia karsholti Toulgoët, 1991 is transferred to Venedictoffia Toulgoët, comb. n., an unrelated genus that is removed from subtribe Arctiina and provisionally placed in the Phaegopterina. Phragmatobia oberthueri Rothschild, 1910, described from Tibet, is a synonym of Lachana alpherakii (Grum-Grzhimailo, 1891) [Erebidae: Lymantriinae], syn. n., comb. n.

CORRELATED EVOLUTION OF FEMALE NEOTENY AND FLIGHTLESSNESS WITH MALE SPERMATOPHORE PRODUCTION IN FIREFLIES (COLEOPTERA: LAMPYRIDAE)

The beetle family Lampyridae (fireflies) encompasses ∼100 genera worldwide with considerable diversity in life histories and signaling modes. Some lampyrid males use reproductive accessory glands to produce spermatophores, which have been shown to increase female lifetime fecundity. Sexual dimorphism in the form of neotenic and flightless females is also common in this family. A major goal of this study was to test a hypothesized link between female flight ability and male spermatophore production. We examined macroevolutionary patterns to test for correlated evolution among different levels of female neoteny (and associated loss of flight ability), male accessory gland number (and associated spermatophore production), and sexual signaling mode. Trait reconstruction on a molecular phylogeny indicated that flying females and spermatophores were ancestral traits and that female neoteny increased monotonically and led to flightlessness within multiple lineages. In addition, male spermatophore production was lost multiple times. Our evolutionary trait analysis revealed significant correlations between increased female neoteny and male accessory gland number, as well as between flightlessness and spermatophore loss. In addition, female flightlessness was positively correlated with the use of glows as female sexual signal. Transition probability analysis supported an evolutionary sequence of female flightlessness evolving first, followed by loss of male spermatophores. These results contribute to understanding how spermatophores have evolved and how this important class of seminal nuptial gifts is linked to other traits, providing new insights into sexual selection and life-history evolution.

The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae)

In order to facilitate the study of the evolution of female flightlessness among the geometrid subfamily Ennominae (Lepidoptera, Geometridae), we carried out a phylogenetic analysis based on a morphological data matrix, and DNA sequences. We used seven nuclear gene fragments, elongation factor 1α (EF-1α), wingless (wgl), isocitrate dehydrogenase (IDH), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), ribosomal protein S5 (RpS5) and segments D1 and D2 of the 28S rRNA gene, and one mitochondrial gene fragment, cytochrome oxidase subunit I (COI). Sampling included 55 species of Ennominae covering all tribes with flightless females of the Holarctic boreal zone, and some other geometrids used as outgroups. Our results clearly confirmed that Ennominae (including Alsophila of the traditional subfamily Alsophilinae) is a monophyletic group, as well as supported the previously established morphology-based division of Ennominae into “ennomine” and “boarmiine” groups of genera. A number of taxonomic ambiguities were resolved but the monophyly of the traditionally recognised tribe Bistonini, comprising a number of flightless species, remained ambiguous. Bistonini is thus suggested to be subsumed to the tribe Boarmiini in the broad sense. Indeed, an analysis of timing of divergence suggested that Boarmiini s. lat. rapidly diversified in the late Oligocene/early Miocene. Within the Ennominae, seven independent origins of female flightlessness were revealed facilitating phylogenetic comparative analyses to be performed in search of causes and consequences of this phenomenon. The present phylogenetic hypothesis supports the conclusions of the “adaptive story”, a hypothesis of the sequence of evolutionary events leading to flightlessness, we have presented earlier ( Snäll et al., 2007). In particular, in the “boarmiine” group, the tribe Boarmiini s. lat. clearly represents a group of geometrids in which female flightlessness has evolved more frequently than in any other tribes, suggesting that this clade has likely been predisposed to evolutionary events leading to the manifestation of female flightlessness. The ancestor of the wing-reduced Ennominae has likely been a winged but slow flying forest moth feeding polyphagously on deciduous trees.

Rapid spatial learning in a velvet ant (Dasymutilla coccineohirta)

Spatial learning has been examined in a variety of animals to determine what cues are used to navigate through a complex environment. A common feature of previously studied vertebrates and invertebrates is their need to return to a previously visited site for mating, nesting, foraging or predator avoidance. Velvet ants (Hymenoptera: Mutillidae) are cursorial parasitoids with flightless females that must walk through complex terrain to find ground dwelling host larvae burrows. Velvet ants are not central-place foragers (they do not return to an established nest site) so much of the previous work on spatial learning does not directly apply in this context. It was assumed that females primarily use chemosensory cues for navigation and burrow location instead of visual learning. This study, however, demonstrates that velvet ant females are able to use visual landmarks to find an inconspicuous exit in an aversion-motivation spatial learning task. A significant number of velvet ants learned to locate the exit after seven training trials and went to the previous location of the exit even after the maze had been rotated, showing that landmarks external to the maze were used to learn the escape location.

Laboratory Evolution of the Migratory Polymorphism in the Sand Cricket: Combining Physiology with Quantitative Genetics

Predicting evolutionary change is the central goal of evolutionary biology because it is the primary means by which we can test evolutionary hypotheses. In this article, we analyze the pattern of evolutionary change in a laboratory population of the wing-dimorphic sand cricket Gryllus firmus resulting from relaxation of selection favoring the migratory (long-winged) morph. Based on a well-characterized trade-off between fecundity and flight capability, we predict that evolution in the laboratory environment should result in a reduction in the proportion of long-winged morphs. We also predict increased fecundity and reduced functionality and weight of the major flight muscles in long-winged females but little change in short-winged (flightless) females. Based on quantitative genetic theory, we predict that the regression equation describing the trade-off between ovary weight and weight of the major flight muscles will show a change in its intercept but not in its slope. Comparisons across generations verify all of these predictions. Further, using values of genetic parameters estimated from previous studies, we show that a quantitative genetic simulation model can account for not only the qualitative changes but also the evolutionary trajectory. These results demonstrate the power of combining quantitative genetic and physiological approaches for understanding the evolution of complex traits.

Glowworms: a review of Arachnocampa spp. and kin

The term 'glowworm' is used in connection with the flightless females of lampyrid fireflies and to describe the luminescent larvae of certain fungus gnats that belong to the subfamilies Arachnocampinae, Keroplatinae and Macrocerinae of the dipteran family Keroplatidae. This review focuses on the luminescent larval fungus gnats. The weakly luminescent species of the Holarctic feed mainly on fungal spores, but some, such as Orfelia fultoni, have turned to a carnivorous diet. Larval Australian and New Zealand Arachnocampa spp. produce brighter in vivo (but not necessarily in vitro) lights, live in cool, damp and dark places and are exclusively predatory. They lure their prey (usually small flying insects) with the help of their blue-green light emissions towards snares consisting of vertical silk threads coated with sticky mucus droplets. Fungus gnats with similar 'fishing lines' are found in the Neotropics, but they are not luminescent. The larval stage is longest in the life cycle of Arachnocampa, lasting up to a year, depending on climatic conditions such as temperature and humidity as well as food supply. In A. luminosa, but not the Australian A. flava, female pupae and even female imagines are luminescent. However, it remains to be demonstrated whether it is the light of the female, a pheromone or both that attract the males. Light organs and the chemical reactions to produce light differ between the holarctic and the Australian/New Zealand species. Prey is attracted only by the glowworm's light; odours of the fishing lines or the glowworms themselves are not involved. Recognition of the prey by the glowworm involves mechano- and chemoreception. The eyes of both larval and adult glowworms are large and functional over a spectral range covering UV to green wavelengths. Adults are poor fliers, live only for a few days, have degenerate mouth parts and do not feed. Maintenance of glowworms in captivity is possible and the impact of tourism on glowworms in natural settings can be minimized through appropriate precautions.

Are polyphagous geometrid moths with flightless females adapted to budburst phenology of local host species?

The majority of studies demonstrating local adaptation of insect herbivores involve sessile species, particularly those with a parthenogentic phase to their life history or endophagous “parasites” of plants. Current arguments suggest the strength of selection determines whether local adaptation can or cannot take place. Therefore local adaptation should not be limited to species with such traits. We studied the ability of three polyphagous geometrid moths with flightless adult females (Erannisdefoliaria, Operophtera brumata and O. fagata) to synchronise their egg hatching with the budburst of a local host species in north east Scotland. A strong selection for hatching time is expected among generalist moths given the large variation in budburst phenology and an inability to hatch in synchrony with budburst decreases moth fitness substantially. In two successive seasons, we trapped emerging females from patches of five host species and recorded the temperature sum needed for 50% egg hatch of each brood laid by the trapped females. The hatching times of broods were compared against the average budburst time of the maternal host species in the study area. In addition, the trapping dates of each female were recorded. Only O. brumata showed synchrony with egg hatch and budburst which suggests local phenological adaptation to different host species. This could be maintained by selection and partial reproductive isolation between populations dwelling on different host species. No phenological adaptation was found in the other common geometrids of the study area.

Rudimentary halteres of some flightless female Phoridae (Diptera) reassessed, and some taxonomic implications

The supposed rudimentary halteres of the flightless females of the Neotropical Ecituncula halterata Borgmeier and genus Pulicimyia Borgmeier are reinterpreted as wing rudiments. Consequently E. halterata is transferred to the genus Ecitophora Schmitz, creating a junior synonym of E. breviptera Disney. Pulicimyia is synonymised with Puliciphora Dahl and the resulting Puliciphora modesta (Borgmeier) comb. nov. makes a homonym with the Afrotropical P. modesta (Disney), which is therefore renamed P. etiamodesta nom. nov. The replacement name P. edaphomyia nom. nov. is proposed for the Afrotropical P. nigriventris (Borgmeier), as the name is preoccupied by an older synonym of a widely distributed Old World species. The Neotropical Homalophora epichaeta Borgmeier is transferred to Puliciphora, with the consequent synonymy of P. mexicanae Disney with this species. The Neotropical P. sobria Borgmeier is reported from the Nearctic Region, and P. cavatica Disney is synonymised with it. P. jacquemarti sp. nov. is described from Puerto Rico. A revised key to Nearctic Puliciphora females is provided.

Life history and osmoregulatory ability of Telmatogeton amphibius (Diptera, Chironomidae) at Marion Island

Although the non-crustacean arthropod fauna of the intertidal zone in the sub-Antarctic is both diverse and abundant, little is known about the biology of the species that occur in this habitat. Here, we provide information on the biology and osmoregulatory ability of the marine intertidal midge Telmatogeton amphibius (Eaton) (Diptera, Chironomidae) at Marion Island. Larval densities of this species in the lower shore zones can be as high as 16,000 individuals m−2 in their preferred habitat during peak abundance in summer. Winter abundances are substantially lower, and adults are much less abundant than larvae. Like other chironomids, this species has four larval instars and the flightless adult females have obligatory parthenogenesis. It is a strong osmoregulator. Larvae show little variation in body mass irrespective of whether they find themselves in freshwater or seawater, or are switched between the media. Haemolymph osmolality [ca. 400 milliosmol (mOsm)] varies by only 61 mOsm over a 1,520 mOsm range of the external medium. T. amphibius is similar in many respects to intertidal telmatogetonine midges found in other geographic regions.

The dorsal abdominal glands and the higher classification of the Phoridae (Diptera)

A brief historical review of the proposed subfamilies and tribes within the Phoridae is provided. The value of the position of the female dorsal abdominal glands in the Metopininae is highlighted. It is proposed that these discharge between tergites 4 and 5 in the thus newly diagnosed Metopinini and between T5 and T6 in the resurrected tribe Gymnophorini, which embraces the Beckerinini of previous authors plus the Megaseliini, which are both synonymised with the newly diagnosed Gymnophorini. This tribe, therefore, now includes more than half the known species of Phoridae. The genus Aenigmatopoeus Schmitz is transferred from the Aenigmatiinae to the Metopininae, Metopinini, thus further undermining the presumed monophyly of the Aenigmatiinae, which may be just a polyphyletic assemblage with convergently similar flightless females.

Revisionary notes on Chonocephalus Wandolleck (Diptera: Phoridae) with keys to species of the Holarctic Region

The minute flies of the sexually dimorphic genus Chonocephalus Wandolleck, with its flightless females and winged males, has long been in taxonomic chaos through more than half the species having been described from one sex only. The previously known species are reviewed, two formerly misidentified species are described and named C. marginatus sp. nov., from India, and C. collini sp. nov., from the Seychelles. Eleven new synonyms are proposed. Two species are declared to be species indeterminata, 6 lectotypes and 2 neotypes are designated. The genus Epichonocephalus Schmitz is synonymised with Chonocephalus. The 43 previously recognised species are thus reduced to 32. Numerous undescribed, and frequently misidentified, species are present in museum collections. As a start to providing new keys to the species of each Biogeographic Region, keys to males and females of the Holarctic Region are provided.

On Research and Entomological Education IV: Quantifying Mate Search in a Perfect Insect-Seeking True Facts and Insight (Coleoptera: Lampyridae, Photinus)

Male Photinus collustrans LeConte fireflies fly over their grassland habitats flashing and seeking their flightless females. I followed individual males, measured, and took note of various aspects of their behavior. Then, from a sample of 255 male runs, with a total distance of 13.9 miles and 10,306 flashes, various sets of these males, those seemingly directed by other than search flight-plans, were removed to leave a sample to characterize pure search flight. Fireflies are good subjects for students to study foraging ecology and sexual selection, and from studies of common grassland fireflies it will be clear to students that even simple behavior by males of a single species, under seemingly uncomplicated and homogeneous conditions, can be complex, but provide opportunity for theoretical and empirical exploration. Among factors identified here as influencing male mate-seeking behavior were ambient temperature, ambient light level, and time of night. Other influencing factors, enigmas, and student explorations are indicated.

Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants.

A generalist feeding strategy is common among eruptive insect herbivores but the ultimate reasons for a generalist strategy are not clear. Although generalist insect herbivores are able to complete their life cycle on several species of host plants, there is wide variation in the performance of individuals grown on different hosts. We examined whether different populations of Operophtera brumata are adapted to use the host species which is locally most abundant, and how the host plant affects growth and development of the insect. We reared two allopatric populations (eastern Finland, Prunus padus; south-west Finland, Quercus robur) on four species of host plants (Pr. padus, Populus tremula, Q. robur, Salix phylicifolia) from neonate larvae to the adult stage and measured the growth and development of individuals and the timing of adult hatching. The performance of both populations was best on Pr. padus, and the south-western population, originally on Q. robur, was well adapted to this host. The host affected the growth of females more than that of males. The host plant had an unexpected effect on hatching times of the adults. Individuals grown on the original host hatched in normal synchrony, i.e. males 6-7 days before females; but on alternative hosts this synchrony was disturbed. As is common in eruptive, capital-breeding generalist moths where female fecundity is linked to weight, host quality is critical for the flightless females of O. brumata. We suggest that in a heterogeneous environment the disturbing effect of alternative host plants on adult emergence may decrease the population density and growth rate compared to the potential maximum in a homogeneous environment.