Subcortical life, evolution of flattened body, and constrained mating posture in the earwig Platylabia major (Insecta: Dermaptera: "Anisolabididae").

Many animals take advantage of the shaded, humid, and protected environments in subcortical spaces, i.e., thin spaces under the loosened bark of dead trees. Permanent inhabitants of subcortical spaces often show specialized morphologies, such as a miniaturized or dorsoventrally flattened body. However, the evolutionary consequences of these specialized morphologies on behavioral, ecological, and life-history traits have been little studied. We studied the mating biology and anatomy of Platylabia major (usually placed in the family Anisolabididae), which is an obligate inhabitant of subcortical spaces with a paper-like flattened body, and compared them with those of two thicker, spongiphorid earwigs, Nesogaster amoenus and Paralabellula curvicauda. Mating trials in various settings showed that Pl. major requires thin spaces sandwiched by two planes to accomplish genital coupling and insemination. In contrast, the thicker species, although also frequently found in subcortical spaces, could mate on a single horizontal plane due to the ability of the male to twist its abdomen through approximately 180°. Examination by micro-computed tomography and a reagent-based clearing technique revealed no substantive differences in the configuration of mid-abdominal musculature between the species. The dorsal and lateral muscles of Pl. major, which are almost parallel to the antero-posterior body axis for accommodation within the thin abdomen, seemed incapable of producing the power to twist the abdomen. The abdominal musculature conforms to a simple pattern in both male and female earwigs, which is repeated in each of the pregenital segments. We conclude that small differences in the range of motion of each abdominal segment can result in large differences in possible mating postures and positions. Surgical experiments also demonstrated that both right and left penises of Pl. major are competent and used for insemination with no lateral bias, as in most other earwigs with twin penises studied to date.

Are males just passive? Coupling mechanism of the Brazilian cave insects with inverted genitalia.

Species of the Brazilian cave barklouse genus Neotrogla (Psocodea: "Psocoptera": Trogiomorpha: Prionoglarididae: Sensitibillini) are known to have a "female penis (gynosome)" that functions as an intromittent organ inserted into the membranous pouches in the simple male genital chamber during copulation to receive semen. However, the functions of other male and female genital structures and the copulatory processes of Neotrogla were completely unknown to date. Based on µCT observation of the male and female postabdomen and connected muscles both before and in copula, we clarified the functions of the male and female genital structures. In addition, based on the analyses of the established 3D models, we concluded that precise and rigid contact of multiple genital structures, and step-by-step releases of each holding mechanism achieved by the cooperation of both sexes are involved in the copulatory processes. The coevolution between the male and female genital structures in Neotrogla may provide a new example for the evolution of tolerance traits.

Identification and reproductive isolation of Euborellia species (Insecta, Dermaptera, Anisolabididae) from East and Southeast Asia.

Euborellia (Anisolabididae: Anisolabidinae) is one of the most speciose genera of earwigs (Dermaptera), and its species-level classification is difficult. To settle the classification of brachypterous species with abbreviated tegmina recorded from East and Southeast Asia, we examined the morphology and reproductive isolation of three tentative Euborellia species, and analyzed the DNA barcoding region of the mitochondrial cytochrome oxidase subunit I (COI) gene. The observed complete reproductive isolation among the three Euborellia taxa and considerable differentiation in the COI sequences clearly show that each should be treated as a separate species. Based on morphology, distribution and the DNA sequence, we identify Euborellia sp. 1 of Malaysia as E.annulata (Fabricius), a circumtropical cosmopolitan with no records of a fully winged form. Samples from Ioto Island (= Iwo-jima Island: Ogasawara Islands, southern Japan) were also identified as this species. Euborellia sp. 3, from the main islands of Japan, was generally larger and lacked a Y-shaped pigmented area on the penis lobe, which is characteristic of Euborellia sp. 1. We propose reinstating E.pallipes (Shiraki) as the oldest name for this taxon. Euborellia sp. 2, even the brachypterous form, can be distinguished from these two species by its paler coloration (particularly the femora), ecarinate post-abdomen, and the shape of the male genitalia (parameres). We tentatively identify this species as E.philippinensis Srivastava based on the morphology of the brachypterous form, although the macropterous form cannot be distinguished from E.femoralis (Dohrn).

A new earwig species of the genus Liparura Burr, 1907 (Dermaptera: Forficulidae) from China.

A new earwig species of the genus Liparura Burr, 1907 of the family Forficulidae, namely L. chongqingensis sp. nov., is described from Chongqing, southwestern China. The new species is characterized by the male forceps basally approached to each other, and each with a small tooth protruding dorsad. A key to the species of Liparura is provided.

Acquisition of novel muscles enabled protruding and retracting mechanisms of female penis in sex-role reversed cave insects.

Brazilian sex-role reversed cave insects (genus Neotrogla) have a striking structure called the gynosome (or female penis), which deeply penetrates male vagina-like genitalia during copulation to receive nutritious semen. However, the protruding and retracting mechanisms of the female penis, including their evolutionary origin, are poorly understood. By using micro-computed tomography (µCT), we compared the genital morphology and musculature between species with a gynosome and others lacking this structure. As a result, we discovered two groups of muscles related to the protrusion and retraction of gynosomes. These muscles were also observed in species with non-protrusible prepenis. This suggests that evolution of these muscles preceded the acquisition of the protruding function of the gynosome, originally having a putative stimulatory function to receive nutritious semen. This intermediate stage probably allowed for the reversal of genital functions.

Klotho protects chromosomal DNA from radiation-induced damage.

Klotho is an anti-aging, single-pass transmembrane protein found mainly in the kidney. Although aging is likely to be associated with DNA damage, the involvement of Klotho in protecting cells from DNA damage is still unclear. In this study, we examined DNA damage in human kidney cells and mouse kidney tissue after ionizing radiation (IR). The depletion and overexpression of Klotho in human kidney cells reduced and increased the cell survival rates after IR, respectively. The formation of γ-H2AX foci, representing DNA damage, was significantly elevated immediately after IR in cells with Klotho depletion and decreased in cells overexpressing Klotho. These results were confirmed in mouse renal tissues after IR. Quantification of DNA damage by a comet assay revealed that the Klotho knockdown significantly increased the amount of DNA damage immediately after IR, suggesting that Klotho protects chromosomal DNA from the induction of damage, rather than facilitating DNA repair. Consistent with this notion, Klotho was detected in both the nucleus and cytoplasm. In the nucleus, Klotho may serve to protect chromosomal DNA from damage, leading to its anti-aging effects.

DNA barcoding of Japanese earwig species (Insecta, Dermaptera), with sequence diversity analyses of three species of Anisolabididae.

Dermaptera is a polyneopteran insect order that includes more than 2,000 described species, commonly known as earwigs, that mainly inhabit tropical, subtropical and warm temperate regions. Although 40 species have been found in Japan, their distribution and habitat preferences have remained ambiguous due to sample misidentification, particularly amongst immature specimens. To overcome this problem, we sequenced and analysed the DNA barcoding region of the mitochondrial cytochrome oxidase I gene (cox1) of dermapteran species recorded from Japan. Including publicly available data, 72.5% of known Japanese dermapteran species were subjected to molecular identification. We extensively sampled three wingless species of subfamily Anisolabidinae (Anisolabididae): Anisolabismaritima, Anisolabellamarginalis and Euborelliapallipes. Although these species exhibit similar habitat preferences as semi-synanthropes, A.maritima, a cosmopolitan species with the highest affinity to seashore, had significantly higher sequence diversity than the latter two species, which are considered endemic to East Asia. A similar trend was observed for (at least partly) winged cosmopolitan species of other families. Introgression with the congener Anisolabisseirokui is also suggested for A.maritima. Possible causes of the varying levels of sequence diversity are discussed.

Potential of Marava arachidis, a Newly Recorded Earwig Species in Egypt as a Biological Control Agent of Rhipicephalus annulatus Tick in Laboratory.

In Egypt, only five species of Dermaptera (earwigs) have been reported. Based on both the morphological and molecular data of the earwig samples collected from a bakery in Beni-Suef, Egypt, we identified the species as Marava arachidis (Spongiphoridae), a cosmopolitan species with no prior records in Egypt. The current study was designed to analyze its predation capability on newly emerged eggs and larvae of the Rhipicephalus annulatus tick. A laboratory functional response study was set up by applying a predation test with various predator-prey ratios as treatments. This experiment was applied using the undefined mix of collected earwigs and the laboratory-collected eggs and the larvae of R. annulatus. The laboratory results showed that the mean number of predated tick eggs was 18.64 ± 11.18 in 24 h under the highest predator-prey ratio (1:10) examined, accompanied by 12.04 ± 4.38 broken but unconsumed eggs. Moreover, M. arachidis predated an average of 12.32 ± 9.07 tick larvae per day. In contrast, the mean dead larvae increased to 38.4 ± 2.30 per day with the highest predator density (1:10). The number of eggs and larvae consumed increased with the predator density. A linear relationship was detected between earwig density and the consumption rates of tick eggs (R2 = 0.99; p = 0.0001) and larvae (R2 = 0.96; p = 0.003). In conclusion, M. arachidis was first recorded in Egypt. This earwig has predation capability on R. annulatus tick eggs and larvae.

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species.

BACKGROUND: The ovipositors of some insects are external female genitalia, which have their primary function to deliver eggs. Drosophila suzukii and its sibling species D. subpulchrella are known to have acquired highly sclerotized and enlarged ovipositors upon their shifts in oviposition sites from rotting to ripening fruits. Inside the ovipositor plates, there are scale-like polarized protrusions termed "oviprovector scales" that are likely to aid the mechanical movement of the eggs. The size and spatial distribution of the scales need to be rearranged following the divergence of the ovipositors. In this study, we examined the features of the oviprovector scales in D. suzukii and its closely related species. We also investigated whether the scales are single-cell protrusions comprised of F-actin under the same conserved gene regulatory network as the well-characterized trichomes on the larval cuticular surface. RESULTS: The oviprovector scales of D. suzukii and D. subpulchrella were distinct in size and spatial arrangement compared to those of D. biarmipes and other closely related species. The scale numbers also varied greatly among these species. The comparisons of the size of the scales suggested a possibility that the apical cell area of the oviprovector has expanded upon the elongation of the ovipositor plates in these species. Our transcriptome analysis revealed that 43 out of the 46 genes known to be involved in the trichome gene regulatory network are expressed in the developing female genitalia of D. suzukii and D. subpulchrella. The presence of Shavenbaby (Svb) or svb was detected in the inner cavity of the developing ovipositors of D. melanogaster, D. suzukii, and D. subpulchrella. Also, shavenoid (sha) was expressed in the corresponding patterns in the developing ovipositors and showed differential expression levels between D. suzukii and D. subpulchrella at 48 h APF. CONCLUSIONS: The oviprovector scales have divergent size and spatial arrangements among species. Therefore, these scales may represent a rapidly diversifying morphological trait of the female reproductive tract reflecting ecological contexts. Furthermore, our results showed that the gene regulatory network underlying trichome formation is also utilized to develop the rapidly evolving trichomes on the oviprovectors of these flies.

Differences in energy source storage in eye stalks between two species of stalk-eyed flies, Sphyracephala detrahens and Cyrtodiopsis dalmanni.

Some diopsid flies have sexually dimorphic eye stalks that are assumed to require considerable nutrition for growth but are advantageous in competition and courtship. According to the handicap theory, the eye span in some dimorphic species serves as a reliable signal of individual quality to an opponent. However, it is not well understood how well eye span represents energy source storage. In this study, we focused on two species: Sphyracephala detrahens, which has weak dimorphism, and Cyrtodiopsis dalmanni, which has moderate dimorphism. We found that the eye stalks of the former species contained more fat bodies than those of the latter species. When the flies were starved, the fat body cells in the eye stalks underwent autophagy. A strong positive correlation was consistently found between eye span and starvation tolerance for S. detrahens, while a weak correlation was found for C. dalmanni. Furthermore, starvation decreased the contest winning rate between S. detrahens pairs with similar eye spans. These findings suggest that the presentation of resource holding potential may be larger than the actual storage ability and that the fidelity of nutritional storage signaling varies; the signal presented by S. detrahens is more reliable than that presented by C. dalmanni.

A standardized nomenclature and atlas of the female terminalia of Drosophila melanogaster.

The model organism Drosophila melanogaster has become a focal system for investigations of rapidly evolving genital morphology as well as the development and functions of insect reproductive structures. To follow up on a previous paper outlining unifying terminology for the structures of the male terminalia in this species, we offer here a detailed description of the female terminalia of D. melanogaster. Informative diagrams and micrographs are presented to provide a comprehensive overview of the external and internal reproductive structures of females. We propose a collection of terms and definitions to standardize the terminology associated with the female terminalia in D. melanogaster and we provide a correspondence table with the terms previously used. Unifying terminology for both males and females in this species will help to facilitate communication between various disciplines, as well as aid in synthesizing research across publications within a discipline that has historically focused principally on male features. Our efforts to refine and standardize the terminology should expand the utility of this important model system for addressing questions related to the development and evolution of animal genitalia, and morphology in general.

A new species of Diplatys (Insecta, Dermaptera, Diplatyidae) earwig from the Western Ghats of India.

To explore diversity of earwigs (Dermaptera) in different agricultural ecosystems of South India, an extensive taxonomic survey was conducted in 2020 during which an undescribed species of Diplatys was collected. Twenty-one species of the genus Diplatys (Diplatyidae, Diplatyinae) have been reported to date from India, of which six species are known from Karnataka, South India. Based on a male specimen collected from a sugarcane field in Karnataka, a new species, Diplatyssahyadriensis sp. nov., is described as the twenty-second species of this genus from India. A revised key to the males of Diplatys species from India and Sri Lanka is provided. This new record adds to the known species diversity in the Sahyadri Ranges of the Western Ghats in Shivamogga District, Karnataka, part of the Southern Plateau and Hills agro-climatic region of India.

Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating.

BACKGROUND: Many male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed remating of the females, resulting in higher paternity. Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and selection on females to increase their mating rate, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to simulate such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating (female trait). Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition. We also analyzed the causes and consequences of this type of traits, taking double receptacles for nutritious seminal gifts, which are known to occur in an insect group with a "female penis" (Neotrogla spp.), as an illustrative example. RESULTS: Our individual-based simulations demonstrated that female-female competition for male-derived nutrients always occur when the environment is oligotrophic and mating costs are low for females. However, a positive correlation between donated gift size and the resultant paternity gain was a requisite for the co-occurrence of large gifts and females' competitive multiple mating for the gifts. When gift donation satisfied female demands and thus resulted in monandry, exaggeration of nuptial gift size also occurred under the assumption that the last male monopolizes paternity. The evolution of double slots for gift acquisition and digestion (female persistence trait) always occurred when males could not satisfy the demands of females for gifts. However, through coevolutionary reduction in male gift size, fixation of this trait in a population drastically reduced the average female fitness. CONCLUSION: Sperm usage patterns, which have rarely been examined for animals with nuptial gifts, can be a critical factor for determining the extent of exaggeration in nuptial gifting. Sex-role reversals in mate competition, as a result of donation of nuptial gifts from males to females, can involve the evolution of male-like, persistent traits in females that reduce population productivity, as is the case with persistence traits in males.

A solution to a sex ratio puzzle in Melittobia wasps.

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Penetration mechanics of elongated female and male genitalia of earwigs.

We unveiled the penile penetration mechanics of two earwig species, Echinosoma horridum, whose intromittent organ, termed virga, is extraordinarily long, and E. denticulatum, whose virga is conversely short. We characterised configuration, geometry, material and bending stiffness for both virga and spermatheca. The short virga of E. denticulatum has a material gradient with the stiffer base, whereas the long virga of E. horridum and the spermathecae of both species are homogeneously sclerotised. The long virga of E. horridum has a lower bending stiffness than the spermatheca. The virga of E. denticulatum is overall less flexible than the spermatheca. We compared our results to a previous study on the penetration mechanics of elongated beetle genitalia. Based on the comparison, we hypothesised that the lower stiffness of the male intromittent organ comparing to the corresponding female structure is a universal prerequisite for the penetration mechanics of the elongated intromittent organ in insects.

A standardized nomenclature and atlas of the male terminalia of Drosophila melanogaster.

Animal terminalia represent some of the most diverse and rapidly evolving structures in the animal kingdom, and for this reason have been a mainstay in the taxonomic description of species. The terminalia of Drosophila melanogaster, with its wide range of experimental tools, have recently become the focus of increased interest in the fields of development, evolution, and behavior. However, studies from different disciplines have often used discrepant terminologies for the same anatomical structures. Consequently, the terminology of genital parts has become a barrier to integrating results from different fields, rendering it difficult to determine what parts are being referenced. We formed a consortium of researchers studying the genitalia of D. melanogaster to help establish a set of naming conventions. Here, we present a detailed visual anatomy of male genital parts, including a list of synonymous terms, and suggest practices to avoid confusion when referring to anatomical parts in future studies. The goal of this effort is to facilitate interdisciplinary communication and help newcomers orient themselves within the exciting field of Drosophila genitalia.

Why Did a Female Penis Evolve in a Small Group of Cave Insects?

The evolution of a female penis is an extremely rare event and is only known to have occurred in a tribe of small cave insects, Sensitibillini (Psocodea: Trogiomorpha: Prionoglarididae). The female penis, which is protrudable and inserted into the male vagina-like cavity during copulation to receive semen, is thought to have evolved independently twice in this tribe, in the Brazilian Neotrogla and the African Afrotrogla. These findings strongly suggest that there are some factors unique to Sensitibillini that have facilitated female penis evolution. Here, several hypothetical factors are presented that may have enabled the evolution of the female penis in Sensitibillini. The female-female competition for nutritious semen, the oligotrophic environment, and the twin insemination slots with switching valve are considered to be the driving factors for female penis evolution. Additionally, the following factors are considered responsible for relaxing the constraint against female penis evolution: preexistence of the female-above mating position, the elongated duct connecting the female pre-penis with the sperm storage organ, and the small male genital cavity accepting the female genital tubercle bearing the opening of this duct. Understanding the factors enabling female penis evolution may also shed light on the evolution of the male penis.

Fitness advantages of the biased use of paired laterally symmetrical penises in an insect.

The evolution of laterality, that is the biased use of laterally paired, morphologically symmetrical organs, has attracted the interest of researchers from a variety of disciplines. It is, however, difficult to quantify the fitness benefits of laterality because many organs, such as human hands, possess multimodal functions. Males of the earwig Labidura riparia (Insecta: Dermaptera: Labiduridae) have morphologically similar laterally paired penises, only one of which is used for inseminating the female during a single copulation bout, and thus provide a rare opportunity to address how selection pressure may shape the evolution of population-level laterality. Our population studies revealed that in 10 populations, located at 2.23-43.3° north, the right penis is predominantly used for copulating (88.6%). A damaged penis was found in 23% of rare left-handers, suggesting that the left penis can function as a spare when the right one is damaged. By pairing L. riparia females with surgically manipulated males, we found that males forced to use the right penis outperformed left-handed males in copulation (the probability of establishing genital coupling during the 1-hr observation period: odds ratio [OR] of 3.50) and insemination (probability of transferring a detectable amount of sperm: OR of 2.94). This right-handed advantage may be due to the coiled morphology of the sperm storage organ with a right-facing opening. Thus, female genital morphology may play a significant role in the evolution of handedness and may have acted as a driving force to reduce penis number in related taxa.

Independent origins of female penis and its coevolution with male vagina in cave insects (Psocodea: Prionoglarididae).

The cave-dwelling psocid tribe Sensitibillini (Afrotrogla, Neotrogla and Sensitibilla) is of special morphological and evolutionary interest because of its possession of reversed copulatory organs: i.e. females of Afrotrogla and Neotrogla have a penis-like organ. The female penis structure is highly variable among taxa, as is the case of the male penis in animals with normal copulatory organs. Here, we present the first molecular phylogeny of Sensitibillini and analyse the evolutionary pattern of their genitalia. Afrotrogla and Neotrogla did not form a monophyletic clade, and their female penis structures are significantly different, suggesting two independent origins of the female penis within Sensitibillini. In Neotrogla, the species that has a simple female penis is embedded among species that have an elaborate penis, and detailed structures of the female penis elaborations are in exact agreement among species, suggesting a secondary simplification of the female penis. A correlated evolutionary pattern between male and female genitalia was also detected. This coevolution of genitalia may suggest that sexual conflict or cryptic 'male' choice drove the diversity of the female penis, as is the case of male penile diversity in animals with conventional genitalia.