Genital Shape Research Articles

The condition-dependence of male genital size and shape.

The male genitals of internal fertilisers evolve rapidly and divergently, and sexual selection is generally responsible for this. Many sexually selected traits are condition-dependent-with their expression dependent upon the resources available to be allocated to them-as revealed by genetic or environmental manipulations of condition. However, it is not clear whether male genitals are also condition-dependent. Here we manipulate condition in two ways (via inbreeding and diet) to test the condition-dependence of the genital arch of Drosophila simulans. We found that genital size but not genital shape suffered from inbreeding depression, whereas genital size and shape were affected by dietary manipulation of condition. The differential effects of these treatments likely reflect underlying genetic architecture that has been shaped by past selection: inbreeding depression is only expected when traits have a history of directional selection, while diet impacts traits regardless of historical selection. Nonetheless, our results suggest genitals can be condition-dependent like other sexually selected traits.

Rapid divergent evolution of internal female genitalia and the coevolution of male genital morphology revealed by micro-computed tomography.

Animal genitalia are thought to evolve rapidly and divergently in response to sexual selection. Studies of genital evolution have focused largely on male genitalia. The paucity of work on female genital morphology is probably due to problems faced in quantifying shape variation, due to their composition and accessibility. Here we use a combination of micro-computed tomography, landmark free shape quantification and phylogenetic analysis to quantify the rate of female genital shape evolution among 29 species of Antichiropus millipedes, and their coevolution with male genitalia. We found significant variation in female and male genital shape among species. Male genital shape showed a stronger phylogenetic signal than female genital shape, although the phylogenetic signal effect sizes did not differ significantly. Male genital shape was found to be evolving 1.2 times faster than female genital shape. Female and male genital shape exhibited strong correlated evolution, indicating that genital shape changes in one sex are associated with corresponding changes in the genital shape of the other sex. This study adds novel insight into our growing understanding of how female genitalia can evolve rapidly and divergently, and highlights the advantages of three-dimensional techniques and multivariate analyses in studies of female genital evolution.

A systemic fungicide might reduce the male genitalia of a stingless bee species by one-third

Bees are essential pollinating insects that significantly contribute to crop production. However, the use of pesticides in modern agriculture has resulted in bees being exposed to a plethora of harmful substances. Larvae of bees are particularly susceptible to exposure, as they can consume contaminated larval food during development. This study opportunely examined the effects of fungicides and insecticides on the size and shape of the genitalia of Scaptotrigona bipunctata (Lepeletier, 1836) males (Hymenoptera: Apidae: Meliponini) during larval development when experimental design was structured to obtain female bees (workers). Therefore, the geometric morphometric analyses were based on male bees that opportunistically emerged. Our findings showed a significant difference in the size of the genitalia of S. bipunctata males exposed to a systemic fungicide during larval development, while the genital shape remained similar. Although the exact impact of these morphological changes on the reproductive success of S. bipunctata males is uncertain, they suggest an adverse effect of pesticides on bees.

Divergence in the internal genital morphology of females and correlated divergence in male intromittent structures among populations of a millipede.

Our understanding of genital evolution comes largely from studies of male genitalia. Females have received far less attention because of the difficulties inherent in quantifying the shapes of their internal genital structures. Here we combine advances in micro-computed tomography with a new landmark free method of quantifying three-dimensional trait shape, to document patterns of divergence in female genital shape, and the correlated divergence of male genitalia among populations of the millipede Antichiropus variabilis. We used single-nucleotide polymorphisms to estimate levels of neutral genetic divergence among seven populations of millipede. Genetic divergence was high and correlated with geographic distance. Comparing phenotypic divergence in genital shape to neutral genetic divergence, we found that genital shape for both females and males has diverged more than would be expected from random drift, consistent with a pattern of directional selection. While there was significant covariation between female and male genital shape across populations, the magnitude of divergence in genital shape between the sexes was not correlated. Our results demonstrate the utility of using three-dimensional scanning technologies to examine female genital traits and add to a small but growing number of studies showing that like male genitalia, female genitalia can be under strong directional selection.

Total evidence analysis elucidates the tangled systematic scenario within Fidicinini (Hemiptera: Auchenorrhyncha, Cicadidae)

The Linnean, Wallacean, and Darwinian shortfalls are knowledge gaps about species taxonomy, distribution, and evolution, respectively. Fidicinini is a tribe of cicadas that suffers from these gaps. We assessed specimens of the tribe sharing similar male genital shape (uncus), but fitting the somatic morphology of either Dorisiana Metcalf, 1952 and Guyalna Boulard & Martinelli, 1996. We build a phylogenetic hypothesis by total evidence analysis and perform a character optimization of the uncus and timbal cover shapes, the last used as diagnostic for both genera. Dorisiana and Guyalna were recovered non-monophyletic. A new genus, Acanthoventrisgen. nov., and ten new species are proposed: A. charrua Ruschel sp. nov., A. claudiae Ruschel sp. nov., A. faustopsaltrius Ruschel sp. nov., A. iara Ruschel sp. nov., A. igneus Ruschel sp. nov., A. olivarius Ruschel sp. nov., A. phoenix Ruschel sp. nov., A. rubemi Ruschel sp. nov., A. tumidus Ruschel sp. nov., and A. viridinotatus Ruschel sp. nov.; and three new combinations A. densusus (Boulard & Martinelli, 2011) comb. nov., A. drewseni (Stål, 1854) comb. nov., and A. jauffreti (Boulard & Martinelli, 2001) comb. nov. We provide illustrated identification keys, occurrence maps, and discuss the distribution of the species in the new genus.

Examining the shape and size of female and male genitalia in snakes using three-dimensional geometric morphometrics

Abstract Quantification of genital variation in males and females can inform our understanding of likely copulatory interactions and evolution of genital diversity. However, no studies have quantified genital shape variation within a single snake species or examined the shape and size of both the vaginal pouch and hemipenes. Here, we examine the shape and size of the genitalia of female and male diamondback water snakes, Nerodia rhombifer, using a three-dimensional automated landmark geometric morphometric approach on models of the lumen of the vaginal pouch and inflated hemipenes, applying these techniques for the first time to the genital shape of vertebrates. Vaginal pouch shape is significantly associated with body size and reproductive status. As females grow larger and become reproductive, the vaginal pouch enlarges, widens and becomes more bifurcated. In reproductive males, the shape of the hemipenes is also significantly associated with body size. As males grow larger, the hemipenes enlarge and widen; their bifurcation becomes more defined and the spines at the base become more prominent. Vaginal pouch and hemipenial centroid size are isometric with respect to body length. The centroid sizes of the hemipenes and vaginal pouch are not significantly different from one another, hence the genitalia match in size. Reproductive females and males covary in the degree of bifurcation and size of their genitalia. We demonstrate the utility of three-dimensional analysis in studies of the shape of soft tissues and advocate its use in future studies of genitalia.

The biology of Simulium noelleri and Simulium dolini: morphological, ecological and molecular data

Molecular genetic research has revolutionized the taxonomy and systematics of the Simuliidae family. Simulium noelleri Friederichs, 1920 is a species of blackfly, common in the Holarctic, reported for 33 countries. In 1954, Topchiev recorded it in Ukraine for the first time. Simulium dolini Usova et Sukhomlin, 1989 has been recorded at the borders of Ukraine and Belarus. It was described for the first time by Usova and Sukhomlin in 1989 from the collection from the territory of Volyn region in 1985. Usova and Sukhomlin, Yankovsky, Adler state that S. noelleri and S. dolini are different species by the morphological characteristics that differ in all phases of development. Adults differ in the structure of the genital appendages, palps, the margin and shape of the face and forehead, the colour of the legs; the larva – in the pattern on the frontal capsule, the number of rays in the fans, mandibular teeth and the hypostoma, the structure of the hind organ of attachment; pupae – in the branching way of gills. Molecular data are becoming an increasingly important tool in insect taxonomy. Therefore, we had to check that these two closely related species also have genetic difference. The development of S. noelleri and S. dolini was studied in four small rivers of Volyn region, Ukraine (Chornohuzka, Konopelka, Putylivka, Omelyanivka) in the period from 2017 to 2019. During initial processing of insect samples, we used the standard protocols EPPO PM7/129. We obtained the nucleotide sequence of S. dolini. It was proved that the populations of S. noelleri and S. dolini from medium and small rivers of Volyn differ in biological, morphological, behavioural and genetic characteristics. Comparison of the species S. noelleri with the data of the GenBank confirms the identification of three distinct morphotypes from Volyn, Great Britain and Canada. As a result of the conducted researches, it was confirmed that two close species of S. dolini and S. noelleri from the noelleri species group differ in the structure of mitochondrial DNA, which confirms their independent taxonomic status. Additional studies comprising more individuals from larger areas of Europe are required to verify the taxonomic position of these two species.

A new Bradophila Marchenkov, 2002 (Copepoda, Cyclopoida, Bradophilidae) parasitic on a flabelligerid polychaete from the Chukchi Sea.

The cyclopoid copepod family Bradophilidae includes a few species of mesoparasitic copepods infecting flabelligerid polychaetes. It contains two species of Bradophila Levinsen, 1878, the type genus: B. pygmaea Levinsen, 1878 and B. minuta Boxshall, O'Reilly, Sikorski & Summerfield, 2019, both known from North Europe. Two other genera (i.e., Trophoniphila M'Intosh, 1885 and Flabellicola Gravier, 1918) have some affinities with this family including their host preference. Mesoparasitic copepods are highly specialized, morphologically reduced forms. Part of their body (endosoma) is partially lodged in the host body and the other part is external (ectosoma); both parts are connected by an intersomital stalk. Infection by these copepods can be readily detected by the presence of the egg-carrying ectosoma on the host external surface. From the analysis of flabelligerid polychaetes collected in 2012 from the Chukchi Sea, two ovigerous female individuals of a bradophilid copepod were recorded. These specimens were recognized as representative of an undescribed species of Bradophila. The new species, B. susanae n. sp., shows the generic diagnostic characters and differs from its two other known congeners in several respects, including the cuticular ectosomal ornamentation, body proportions, size of the intersomital stalk, position of the genital pore, and shape and arrangement of egg sacs. Also, the new species ectosomal size range (0.440 - 0.450 μm) falls between the size range of its two known congeners. Our finding expands the known host range of bradophilid copepods to include a new flabelligerid host, Bradabyssa nuda (Annenkova-Chlopina) from the Russsian Arctic region.

3D genital shape complexity in female marine mammals.

Comparisons of 3D shapes have recently been applied to diverse anatomical structures using landmarking techniques. However, discerning evolutionary patterns can be challenging for structures lacking homologous landmarks. We used alpha shape analyses to quantify vaginal shape complexity in 40 marine mammal specimens including cetaceans, pinnipeds, and sirenians. We explored phylogenetic signal and the potential roles of natural and sexual selection on vaginal shape evolution. Complexity scores were consistent with qualitative observations. Cetaceans had a broad range of alpha complexities, while pinnipeds were comparatively simple and sirenians were complex. Intraspecific variation was found. Three‐dimensional surface heat maps revealed that shape complexity was driven by invaginations and protrusions of the vaginal wall. Phylogenetic signal was weak and metrics of natural selection (relative neonate size) and sexual selection (relative testes size, sexual size dimorphism, and penis morphology) did not explain vaginal complexity patterns. Additional metrics, such as penile shape complexity, may yield interesting insights into marine mammal genital coevolution. We advocate for the use of alpha shapes to discern patterns of evolution that would otherwise not be possible in 3D anatomical structures lacking homologous landmarks.

The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei.

The shape of the male genitalia in many taxa is the most rapidly evolving morphological structure, often driving reproductive isolation, and is therefore widely used in systematics as a key character to distinguish between sibling species. However, only a few studies have used the genital arch of the male copulatory organ as a model to study the genetic basis of species-specific differences in the Drosophila copulatory system. Moreover, almost nothing is known about the effects of the sex chromosomes on the shape of the male mating organ. In our study, we used a set of crosses between D. virilis and D. lummei and applied the methods of quantitative genetics to assess the variability of the shape of the male copulatory organ and the effects of the sex chromosomes and autosomes on its variance. Our results showed that the male genital shape depends on the species composition of the sex chromosomes and autosomes. Epistatic interactions of the sex chromosomes with autosomes and the species origin of the Y-chromosome in a male in interspecific crosses also influenced the expression of species-specific traits in the shape of the male copulatory system. Overall, the effects of sex chromosomes were comparable to the effects of autosomes despite the great differences in gene numbers between them. It may be reasonably considered that sexual selection for specific genes associated with the shape of the male mating organ prevents the demasculinization of the X chromosome.

High variation in last male sperm precedence and genital morphology in the emerald damselfly, Lestes sponsa

Abstract In organisms in which individuals mate multiply, knowledge of the proportion of offspring sired by the last male to mate (P2) under field conditions is important for a thorough understanding of how sexual selection works in nature. In many insect groups, pronounced intraspecific variation in P2 is commonplace. Interestingly, however, in stark contrast to these observations, compilation of P2 data in dragonflies and damselflies (Odonata) indicates that a high P2, seldom below 0.95, is a feature of this taxon. Here we used double digest restriction-site associated DNA sequencing to generate a panel of single nucleotide polymorphisms (SNPs) with which we could determine paternity and estimate values of P2 in the offspring of 19 field-collected pairs of the emerald damselfly Lestes sponsa. We also estimated the relationship between P2 and male genital shape of 16 males using geometric morphometric analysis. P2 was variable (range = 0.0–1.0; mean = 0.5), and there was a marginally non-significant (P = 0.069) relationship between genital shape and P2, suggesting that males with a high P2 had an aedeagus with a broader tip. We suggest that the high P2-values reported in past studies in Odonata are partly due to the methods used to infer paternity. Use of SNPs to determine patterns of paternity and P2 in odonates is needed for a better appraisal of fitness in odonates, and would open many future avenues for use of odonates as models of sexual selection.

Multivariate stabilizing sexual selection and the evolution of male and female genital morphology in the red flour beetle.

Male genitals are highly divergent in animals with internal fertilization. Most studies attempting to explain this diversity have focused on testing the major hypotheses of genital evolution (the lock‐and‐key, pleiotropy, and sexual selection hypotheses), and quantifying the form of selection targeting male genitals has played an important role in this endeavor. However, we currently know far less about selection targeting female genitals or how male and female genitals interact during mating. Here, we use formal selection analysis to show that genital size and shape is subject to strong multivariate stabilizing sexual selection in both sexes of the red flour beetle, Tribolium castaneum. Moreover, we show significant sexual selection on the covariance between the sexes for specific aspects of genital shape suggesting that male and female genitalia also interact to determine the successful transfer of a spermatophore during mating. Our work therefore highlights the important role that both male and female genital morphologies play in determining mating success and that these effects can occur independently, as well as through their interaction. Moreover, it cautions against the overly simplistic view that the sexual selection targeting genital morphology will always be directional in form and restricted primarily to males.

Female genitalia can evolve more rapidly and divergently than male genitalia

Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice.

Variability and asymmetry in the shape of the spiny dogfish vagina revealed by 2D and 3D geometric morphometrics

AbstractGenital structures are among the most variable in nature and have been suggested to evolve at exceptionally high rates. However, the vast majority of research on genital morphology has been done on male genitalia. We present one of the few studies of female genital shape using geometric morphometrics, and the first of such studies to employ 3D geometric morphometrics, using the spiny dogfish shark, a taxon for which reproductive biology is well‐studied. In a sample of 21 adult females, we found no correlation between body size and reproductive and non‐reproductive trait size, and therefore no general allometric patterns. Furthermore, we found limited evidence for different 2D and 3D vaginal shapes in visibly pregnant and not visibly pregnant sharks, but trends were more obvious in 3D than 2D. We found high congruence between data derived using 2D geometric morphometrics with that derived from 3D methods. We also found exceptionally high asymmetry in the vagina, again more apparent in 3D than in 2D. Visibly pregnant sharks had especially high directional asymmetry (>48% of total variation) likely as a result of an asymmetric distribution of pups in the shark's paired oviducts. Therefore, this asymmetry was functional rather than developmental and presents an important consideration when studying vaginal shape. The lack of significant association between pregnancy and vaginal shape in a species with an extremely long pregnancy suggests that vaginal shape differences may be under additional selective forces such as sexual antagonism during copulation. A combination of 3D geometric morphometric methods along with assessments of asymmetry sheds further light on the growing appreciation that female genitalia is highly variable in shape and may play a substantial role in sexual selection.

Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila

The rapid diversification of sexual traits is a common phenomenon accompanying the evolution of reproductive isolation, yet the evolutionary mechanisms driving such diversification are often unknown. Based on experimentally evolved strains of two sister species of cactophilic Drosophila, we investigated the correlated evolution of primary and secondary sexual traits to semi-natural environments enriched in secondary metabolites. We compared patterns of morphological evolution in the size and shape of male wing and genitalia of Drosophila buzzatii and Drosophila koepferae selected for different levels of alkaloid intensities for 20 generations. We found similar modes of selection operating among organs but not among species. The evolution of these traits in D. koepferae were compatible with patterns of stabilizing selection, while in D. buzzatii were characterized by directional changes. We also found that allometric variation was an important component of genital shape evolution, whereas changes in the wing morphology were less pronounced and mostly non-allometric. Overall, our data suggest that the diversification of sexual traits in this species pair is related to the evolution of dissimilar genetic architectures and reinforced by divergent ecological responses.

Alpha shapes: determining 3D shape complexity across morphologically diverse structures

BackgroundFollowing recent advances in bioimaging, high-resolution 3D models of biological structures are now generated rapidly and at low-cost. To use this data to address evolutionary and ecological questions, an array of tools has been developed to conduct shape analysis and quantify topographic complexity. Here we focus particularly on shape techniques applied to irregular-shaped objects lacking clear homologous landmarks, and propose a new ‘alpha-shapes’ method for quantifying 3D shape complexity.MethodsWe apply alpha-shapes to quantify shape complexity in the mammalian baculum as an example of a morphologically disparate structure. Micro- computed-tomography (μCT) scans of bacula were conducted. Bacula were binarised and converted into point clouds. Following application of a scaling factor to account for absolute size differences, a suite of alpha-shapes was fitted per specimen. An alpha shape is formed from a subcomplex of the Delaunay triangulation of a given set of points, and ranges in refinement from a very coarse mesh (approximating convex hulls) to a very fine fit. ‘Optimal’ alpha was defined as the refinement necessary in order for alpha-shape volume to equal CT voxel volume, and was taken as a metric of overall ‘complexity’.ResultsOur results show that alpha-shapes can be used to quantify interspecific variation in shape ‘complexity’ within biological structures of disparate geometry. The ‘stepped’ nature of alpha curves is informative with regards to the contribution of specific morphological features to overall ‘complexity’. Alpha-shapes agrees with other measures of complexity (dissection index, Dirichlet normal energy) in identifying ursid bacula as having low shape complexity. However, alpha-shapes estimates mustelid bacula as being most complex, contrasting with other shape metrics. 3D fractal dimension is identified as an inappropriate metric of complexity when applied to bacula.ConclusionsAlpha-shapes is used to calculate ‘optimal’ alpha refinement as a proxy for shape ‘complexity’ without identifying landmarks. The implementation of alpha-shapes is straightforward, and is automated to process large datasets quickly. We interpret alpha-shapes as being particularly sensitive to concavities in surface topology, potentially distinguishing it from other shape complexity metrics. Beyond genital shape, the alpha-shapes technique holds considerable promise for new applications across evolutionary, ecological and palaeoecological disciplines.

The evolution of relative trait size and shape: insights from the genitalia of dung beetles.

Insects show relatively little genital variation within species compared to extraordinary and often rapid diversification among species. It has been suggested that selection for reproductive isolation through differences in genital shape might explain this phenomenon. This hypothesis predicts that populations diverge faster in genital shape than in genital size. We tested this prediction in males from 10 dung beetle species with known phylogenetic relationships from the genus Onthophagus (Coleoptera: Scarabaeidae), including four species for which we were able to sample multiple populations. Specifically, we compared intra- and interspecific differentiation in shape and relative sizes of genitalia and calculated their respective evolutionary rates. We compared these rates to two similarly sized non-genital traits, the head and the fore-tibia. We found significant intraspecific variation in genital shape in all four species for which multiple populations were sampled, but for three of them we also identified significant relative size variation. We also found that genital shape evolved at higher rates than relative genital size. Genital shape evolved faster than head shape, but not fore-tibia shape. However, shapes of all measured structures evolved faster than their relative size. We discuss the functional constraints that may bias the developmental evolution of relative size and shape of genitalia and other morphological traits.

Differential Rates of Male Genital Evolution in Sibling Species of Drosophila

Fil: Stefanini, Manuel Ignacio. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Oficina de Coordinacion Administrativa Ciudad Universitaria. Instituto de Ecologia, Genetica y Evolucion de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecologia, Genetica y Evolucion de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecologia, Genetica y Evolucion; Argentina

The evolution of genital shape variation in female cetaceans.

Male genital diversification is likely the result of sexual selection. Female genital diversification may also result from sexual selection, although it is less well studied and understood. Female genitalia are complex among whales, dolphins, and porpoises, especially compared to other vertebrates. The evolutionary factors affecting the diversity of vaginal complexity could include ontogeny, allometry, phylogeny, sexual selection, and natural selection. We quantified shape variation in female genitalia using 2D geometric morphometric analysis, and validated the application of this method to study soft tissues. We explored patterns of variation in the shape of the cervix and vagina of 24 cetacean species (n = 61 specimens), and found that genital shape varies primarily in the relative vaginal length and overall aspect ratio of the reproductive tract. Extensive genital shape variation was partly explained by ontogenetic changes and evolutionary allometry among sexually mature cetaceans, whereas phylogenetic signal, relative testis size, and neonate size were not significantly associated with genital shape. Female genital shape is diverse and evolves rapidly even among closely related species, consistent with predictions of sexual selection models and with findings in invertebrate and vertebrate taxa. Future research exploring genital shape variation in 3D will offer new insights into evolutionary mechanisms because internal vaginal structures are variable and can form complex spirals.

Heterospecific mating between distantly related species of stink bugs and its evolutionary implications

ABSTRACTThe copulatory process in animals is preceded by a series of integrated communication processes which are often under selection to guarantee species-specific courtship and copula. However, individuals of species supposedly in reproductive isolation frequently copulate in nature, which has sparked the attention of evolutionary biologists for decades. While studies on this topic have strongly focused on recently diverged species or populations, few instances of heterospecific copula between distantly related species are known. Here we report an intriguing case of interspecific copula between two distantly related species of stink bugs in nature. We replicated this observation in laboratory conditions and revealed an asymmetric relation: males of Chinavia obstinata copulated with females of C. erythrocnemis but the reverse combination did not occur. We propose a series of hypotheses to explain our observations in the light of the current knowledge on mate recognition and reproductive isolation in stink bugs, considering the potential pre- and postcopulatory barriers involved. Once these two species have probably evolved in allopatry and contacted secondarily, the absence of directional selection against mating signals differentiation is a probable process. We argue that similarities in genital shape and size, most likely a result of convergent evolution, may have played a fundamental role in guaranteeing that these species achieved proper coupling.