Male genital morphology and its influence on female mating preferences and paternity success in guppies

In internally fertilizing species male genitalia often show a higher degree of elaboration than required for simply transferring sperm to females. Among the hypotheses proposed to explain such diversity, sexual selection has received the most empirical support, with studies revealing that genital morphology can be targeted by both pre-and postcopulatory sexual selection. Until now, most studies have focused on these two episodes of selection independently. Here, we take an alternative approach by considering both components simultaneously in the livebearing fish, Poecilia reticulata. We allowed females to mate successively (and cooperatively) with two males and determined whether male genital length influenced the female's propensity to mate with a male (precopulatory selection, via female choice) and whether male genital size and shape predicted the relative paternity share of subsequent broods (postcopulatory selection, via sperm competition/cryptic female choice). We found no evidence that either episode of sexual selection targets male genital size or shape. These findings, in conjunction with our recent work exposing a role of genital morphology in mediating unsolicited (forced) matings in guppies, further supports our prior speculation that sexual conflict may be an important broker of genital evolution in this species.     

Adaptation versus pleiotropy: why do males harm their mates?

Recent studies have documented male traits that cause physicalharm to their mates during copulation. Such harm has been suggestedto either (1) arise as a negative pleiotropic side effect ofadaptations that give males a reproductive advantage in anothercontext or (2) represent a male adaptation per se. In otherwords, male traits that cause harm to their mates may becomeestablished despite the fact that they cause harm or becausethey do so. A critical assumption of the latter hypotheses isthat females respond to infliction of harm in a manner thatis beneficial to their mates: by reducing their propensity toremate and/or by elevating their current reproductive rate.In the present study, we test this assumption by experimentallyinflicting various forms of harm to females immediately aftercopulation in three different insect species. We reveal thatfemales do not delay remating or increase their reproductiverate after being harmed but, on the contrary, remate soonerand lay fewer eggs in some cases. We conclude that selectionfor infliction of harm to females per se is unlikely. Instead,available empirical evidence supports the hypothesis that harmfulmale traits arise as negative pleiotropic side effects of adaptationsthat yield other selective advantages to males during reproductivecompetition.     

Coevolution of male and female genitalia in stalk-eyed flies (Diptera: Diopsidae)

The present study investigates the coevolution of a particular male genital process and the female spermathecal ducts in a clade of stalk-eyed flies (Diptera, Diopsidae) and debates the underlying evolutionary mechanisms. The fine morphology and interaction of the male and female genitalic structures are reconstructed from serial sections of mating pairs in one of the species. It is found that the male genital process traverses the common spermathecal duct to enter the base of one of the separate spermathecal ducts during the mating. Spermatozoa and accessory secretions are not transferred through the male genital process but can be discharged only from the male gonopore near its base. A detailed morphometric study reveals low intraspecific variation and hypoallometry of the male genital process. Across 17 species studied comparatively, the lengths of the male genital process and the female common and separate spermathecal ducts are highly variable. The length of the male genital process is correlated significantly with that of the female common spermathecal duct, but not with that of the separate spermathecal ducts. Based on the combined evidence it is concluded that the male genital process and the female common spermathecal duct have coevolved, and that sexual selection by cryptic female choice constitutes a possible and parsimonious explanation for their coevolution. Alternative or additional explanations in terms of sexually antagonistic coevolution cannot be ruled out conclusively, but are not supported by the available evidence.     

Female genital cutting: a harmless practice?

A recent article in Medical Anthropology Quarterly (Obermeyer 1999) argues that the "facts" about the "harmful effects" of female genital cutting (FGC) are "not sufficiently supported by the evidence" (p. 79). The article suggests three further hypotheses, among others: (1) FGC may be of minimal harm because the more educated continue the practice just as much as the less educated; (2) FGC may be of minimal harm because it is so widespread and persistent; (3) FGC may be of minimal harm because the supposed link between the clitoris and female sexual pleasure is a social construction rather than a physiological reality. I challenge these hypotheses. I say that by appropriate standards of evaluation, FGC is harmful. Finally, I submit that most FGC is a proper matter of concern because it is the irreversible reduction of a human capacity in the absence of meaningful consent.     

No evidence for external genital morphology affecting cryptic female choice and reproductive isolation in Drosophila

Genitalia are one of the most rapidly diverging morphological features in animals. The evolution of genital morphology is proposed to be driven by sexual selection via cryptic female choice, whereby a female selectively uptakes and uses a particular male's sperm on the basis of male genital morphology. The resulting shifts in genital morphology within a species can lead to divergence in genitalia between species, and consequently to reproductive isolation and speciation. Although this conceptual framework is supported by correlative data, there is little direct empirical evidence. Here, we used a microdissection laser to alter the morphology of the external male genitalia in Drosophila, a widely used genetic model for both genital shape and cryptic female choice. We evaluate the effect of precision alterations to lobe morphology on both interspecific and intraspecific mating, and demonstrate experimentally that the male genital lobes do not affect copulation duration or cryptic female choice, contrary to long‐standing assumptions regarding the role of the lobes in this model system. Rather, we demonstrate that the lobes are essential for copulation to occur. Moreover, slight alterations to the lobes significantly reduced copulatory success only in competitive environments, identifying precopulatory sexual selection as a potential contributing force behind genital diversification.     

Evaluating the post‐copulatory sexual selection hypothesis for genital evolution reveals evidence for pleiotropic harm exerted by the male genital spines of Drosophila ananassae

The contemporary explanation for the rapid evolutionary diversification of animal genitalia is that such traits evolve by post‐copulatory sexual selection. Here, we test the hypothesis that the male genital spines of Drosophila ananassae play an adaptive role in post‐copulatory sexual selection. Whereas previous work on two Drosophila species shows that these spines function in precopulatory sexual selection to initiate genital coupling and promote male competitive copulation success, further research is needed to evaluate the potential for Drosophila genital spines to have a post‐copulatory function. Using a precision micron‐scale laser surgery technique, we test the effect of spine length reduction on copulation duration, male competitive fertilization success, female fecundity and female remating behaviour. We find no evidence that male genital spines in this species have a post‐copulatory adaptive function. Instead, females mated to males with surgically reduced/blunted genital spines exhibited comparatively greater short‐term fecundity relative to those mated by control males, indicating that the natural (i.e. unaltered) form of the trait may be harmful to females. In the absence of an effect of genital spine reduction on measured components of post‐copulatory fitness, the harm seems to be a pleiotropic side effect rather than adaptive. Results are discussed in the context of sexual conflict mediating the evolution of male genital spines in this species and likely other Drosophila.     

One tool, many uses: precopulatory sexual selection on genital morphology in Aquarius remigis

While congruent evidence indicates that sexual selection is the most likely selective force explaining the rapid divergence of male genital morphology in insects, the mechanisms involved in this process remain unclear. In particular, little attention has been paid to precopulatory sexual selection. We examine sexual selection for mating success on male genital components in six populations of Aquarius remigis, a water strider characterized by unique genital morphology. Multivariate selection analysis confirms previous findings that precopulatory sexual selection favours longer external genitalia, and provides new evidence that this selection acts independently on external genital components. In contrast, the size of the major internal genital sclerite is not correlated with mating success. Thus, precopulatory sexual selection acts strongly on the size of the external genitalia, but not on the intromittent organ itself. These results highlight the multiple functions of genital organs and the importance of both precopulatory and post-copulatory sexual selection in shaping the remarkable diversity of male genitalia in insects.     

Genital cutting and western discourses on sexuality

This article explores dominant discourses surrounding male and female genital cutting. Over a similar period of time, these genital operations have separately been subjected to scrutiny and criticism. However, although critiques of female circumcision have been widely taken up, general public opinion toward male circumcision remains indifferent. This difference cannot merely be explained by the natural attributes and effects of these practices. Rather, attitudes toward genital cutting reflect historically and culturally specific understandings of the human body. In particular, I suggest that certain problematic understandings of male and female sexuality are deeply implicated in the dominant Western discourses on genital surgery.     

Linear and Machine Learning modelling for spatiotemporal disease predictions: Force-of-Infection of Chagas disease

BackgroundChagas disease is a long-lasting disease with a prolonged asymptomatic period. Cumulative indices of infection such as prevalence do not shed light on the current epidemiological situation, as they integrate infection over long periods. Instead, metrics such as the Force-of-Infection (FoI) provide information about the rate at which susceptible people become infected and permit sharper inference about temporal changes in infection rates. FoI is estimated by fitting (catalytic) models to available age-stratified serological (ground-truth) data. Predictive FoI modelling frameworks are then used to understand spatial and temporal trends indicative of heterogeneity in transmission and changes effected by control interventions. Ideally, these frameworks should be able to propagate uncertainty and handle spatiotemporal issues.Methodology/principal findingsWe compare three methods in their ability to propagate uncertainty and provide reliable estimates of FoI for Chagas disease in Colombia as a case study: two Machine Learning (ML) methods (Boosted Regression Trees (BRT) and Random Forest (RF)), and a Linear Model (LM) framework that we had developed previously. Our analyses show consistent results between the three modelling methods under scrutiny. The predictors (explanatory variables) selected, as well as the location of the most uncertain FoI values, were coherent across frameworks. RF was faster than BRT and LM, and provided estimates with fewer extreme values when extrapolating to areas where no ground-truth data were available. However, BRT and RF were less efficient at propagating uncertainty.Conclusions/significanceThe choice of FoI predictive models will depend on the objectives of the analysis. ML methods will help characterise the mean behaviour of the estimates, while LM will provide insight into the uncertainty surrounding such estimates. Our approach can be extended to the modelling of FoI patterns in other Chagas disease-endemic countries and to other infectious diseases for which serosurveys are regularly conducted for surveillance.     

Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9- and beta1 integrin-mediated pathway

Tuberculous granulomas are the sites of interaction between the host response and the tubercle bacilli within infected individuals. They mainly consist of organized aggregations of lymphocytes and macrophages (Mf). A predominant role of mycobacterial envelope glycolipids in granulomas formation has been recently emphasized, yet the signaling events interfering with granuloma cell differentiation remain elusive. To decipher this molecular machinery, we have recently developed an in vitro human model of mycobacterial granulomas. In this study, we provide evidence that the mycobacterial proinflammatory phosphatidyl-myo-inositol mannosides and lipomannans (LM), as well as the anti-inflammatory lipoarabinomannan induce granuloma formation, yet only the proinflammatory glycolipids induce the fusion of granuloma Mf into multinucleated giant cells (MGC). We also demonstrate that LM induces large MGC resembling those found in vivo within the granulomas of tuberculosis patients, and that this process is mediated by TLR2 and is dependent on the beta(1) integrin/ADAM9 cell fusion machinery. Our results demonstrate for the first time that the Mf differentiation stage specifically occurring within granulomatous structures (i.e., MGC formation) is triggered by mycobacterial envelope glycolipids, which are capable of inducing the cell fusion machinery. This provides the first characterization of the ontogeny of human granuloma MGC, thus resulting in a direct modulation by a particular mycobacterial envelope glycolipid of the differentiation process of granuloma Mf.     

Involvement of the purinergic P2X7 receptor in the formation of multinucleated giant cells

Multinucleated giant cells (MGC), a hallmark of chronic inflammatory reactions, remain an enigma of cell biology. There is evidence implicating the purinergic P2X7 receptor in the fusion process leading to MGC. To investigate this, we used HEK 293 cells stably transfected with either 1) the full-length rat P2X7 receptor (P2X7 cells), 2) a rat P2X7 receptor lacking the C-terminal domain (P2X7TC), or 3) a mock vector, and rat alveolar macrophages (MA) expressing the native receptor. P2X7 cells cultured in serum-free medium formed increased numbers of MGC and displayed a higher fusion index compared with mock transfectants. Stimulation of P2X7 pore-forming activity in P2X7 cells by polymyxin B (PMB) further increased significantly the formation of MGC. Conversely, blockers of P2X-receptors including oxidized ATP, brilliant blue G, and pyridoxal phosphate-6-azophenyl-2'-4'-disulfonic acid inhibited significantly MGC formation in both unstimulated and PMB-stimulated P2X7-transfected cells. In contrast, cells transfected with the truncated P2X7TC were devoid of pore-forming activity, did not respond to PMB stimulation, and failed to form enhanced numbers of MGC, thus behaving as mock transfectants. As found for P2X7-transfected cells, PMB also potentiated dose-dependently the formation of multinucleated MA by rat alveolar MA. Pretreatment with oxidized ATP abrogated the PMB stimulatory effects. Together, these data demonstrate unequivocally the participation of P2X7 receptor in the process of MGC formation. Our study also provides evidence suggesting that stimulation of the P2X7 receptor pathway in MA may mediate increased formation of MGC during chronic inflammatory reactions.     

Experimental reduction of intromittent organ length reduces male reproductive success in a bug

It is now clear in many species that male and female genital evolution has been shaped by sexual selection. However, it has historically been difficult to confirm correlations between morphology and fitness, as genital traits are complex and manipulation tends to impair function significantly. In this study, we investigate the functional morphology of the elongate male intromittent organ (or processus) of the seed bug Lygaeus simulans, in two ways. We first use micro-computed tomography (micro-CT) and flash-freezing to reconstruct in high resolution the interaction between the male intromittent organ and the female internal reproductive anatomy during mating. We successfully trace the path of the male processus inside the female reproductive tract. We then confirm that male processus length influences sperm transfer by experimental ablation and show that males with shortened processi have significantly reduced post-copulatory reproductive success. Importantly, male insemination function is not affected by this manipulation per se. We thus present rare, direct experimental evidence that an internal genital trait functions to increase reproductive success and show that, with appropriate staining, micro-CT is an excellent tool for investigating the functional morphology of insect genitalia during copulation.     

The evolution of male genitalia: functional integration of genital sclerites in the dung beetle Onthophagus taurus

It is now widely recognized that sexual selection has been important in the rapid and divergent evolution of male genital morphology. However, distinguishing among putative mechanisms of sexual selection acting on male genital morphology represents a considerable challenge. Although there is growing evidence that variation in the size and/or shape of male genital structures can determine a male's success in gaining fertilizations, our knowledge of the functional morphology of male genitalia remains limited. Here we examine the functional morphology of genital sclerites that are known to influence paternity in the dung beetle Onthophagus taurus . We show that three of the sclerites form a functionally integrated unit that generates the tubular-shaped spermatophore and delivers its opening to the female's spermathecal duct. A fourth sclerite acts as a holdfast device during copulation. Our observations shed light on the mechanism by which these sclerites influence a male's paternity, and their patterns of phenotypic and genetic (co)variation.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 257–266.     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

Sexual selection and genital evolution

Genitalia are conspicuously variable, even in closely related taxa that are otherwise morphologically very similar. Explaining genital diversity is a longstanding problem that is attracting renewed interest from evolutionary biologists. New studies provide ever more compelling evidence that sexual selection is important in driving genital divergence. Importantly, several studies now link variation in genital morphology directly to male fertilization success, and modern comparative techniques have confirmed predicted associations between genital complexity and mating patterns across species. There is also evidence that male and female genitalia can coevolve antagonistically. Determining mechanisms of genital evolution is an important challenge if we are to resolve current debate concerning the relative significance of mate choice benefits and sexual conflict in sexual selection.     

Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells

Cumulus cells and mural granulosa cells (MGC) are phenotypically different and there is now evidence suggesting that the oocyte plays an active role in determining the fate of follicular somatic cells. This study investigates the role of oocyte-secreted factor(s) in the regulation of the growth and differentiation of cumulus and MGC. Bovine cumulus-oocyte complexes (COC) and MGC were cultured with various hormones for 18 h followed by a further 6-h pulse of [(3)H]thymidine as an indicator of follicular cell DNA synthesis. The COC incorporated 11 to 14 times more [(3)H]thymidine than MGC in either the absence or presence of 50 ng/ml insulin-like growth factor (IGF)-I. Purified porcine FSH (450 ng/ml) added together with IGF-I marginally increased (3)H incorporation in MGC relative to IGF-I alone but dramatically decreased incorporation in COC sixfold. Conversely, mean progesterone production in the presence of IGF-I + FSH was 13-fold higher from MGC than from COC, confirming a distinctive phenotype of cumulus cells. However, this phenotype was found to be dependent on the presence of the oocyte, as microsurgical removal of the oocyte (oocytectomy) resulted in an 11-fold decrease in [(3)H]thymidine incorporation in cumulus cells treated with IGF-I, elimination of the inhibitory effect of FSH on IGF-I-stimulated DNA synthesis, and led to a 2-fold increase in progesterone production in medium with IGF-I and FSH. All of these markers were completely restored to COC levels when oocytectomized complexes were cocultured with denuded oocytes (DO) at a concentration of 0.5 oocytes/microl, demonstrating that oocytes secrete a soluble factor(s) that promotes growth and attenuates cumulus cell progesterone secretion. In the presence of IGF-I, [(3)H]thymidine incorporation in MGC increased ninefold above control levels with the addition of DO. The addition of FSH to IGF-I-increased (3)H counts in MGC, however, led to a decrease in counts in MGC + DO as is also observed in COC. Furthermore, progesterone production was halved when DO were added to MGC cultures, most notably in the presence of IGF-I and/or FSH. These results provide further evidence that MGC and cumulus cells have distinctive phenotypes and that the oocyte is responsible for some of the characteristic features of cumulus cells. Bovine oocytes secrete a soluble factor(s) that simultaneously promotes growth and attenuates steroidogenesis in follicular somatic cells.     

Sex‐biased dispersal,kin selection and the evolution of sexual conflict

There is growing interest in resolving the curious disconnect between the fields of kin selection and sexual selection. Rankin's (2011, J. Evol. Biol. 24 , 71–81) theoretical study of the impact of kin selection on the evolution of sexual conflict in viscous populations has been particularly valuable in stimulating empirical research in this area. An important goal of that study was to understand the impact of sex‐specific rates of dispersal upon the coevolution of male‐harm and female‐resistance behaviours. But the fitness functions derived in Rankin's study do not flow from his model's assumptions and, in particular, are not consistent with sex‐biased dispersal. Here, we develop new fitness functions that do logically flow from the model's assumptions, to determine the impact of sex‐specific patterns of dispersal on the evolution of sexual conflict. Although Rankin's study suggested that increasing male dispersal always promotes the evolution of male harm and that increasing female dispersal always inhibits the evolution of male harm, we find that the opposite can also be true, depending upon parameter values.     

Molecular phylogeny reveals the repeated evolution of complex male genital traits in the New Zealand moth genus Izatha (Lepidoptera: Xyloryctidae)

Male genitalia are among the most rapidly evolving and divergent morphological structures and sexual selection is known to drive this phenomenon in many taxa. Because of their diversity, even within a single genus, genital characters are frequently used to infer relationships among closely‐related species. Moths within the genus Izatha (Xyloryctidae) are ideal candidates for investigating the phylogenetic patterns of genital evolution as they display great variation in male genital structure and complexity. We determined the evolutionary relationships among 31 species of Izatha by constructing a molecular phylogeny of the genus based on the mitochondrial cytochrome oxidase subunit I gene and the isocitrate dehydrogenase and carbamoylphosphate synthase domain protein nuclear genes. This allowed estimations of ancestral male genital character states and patterns of male genital diversification using maximum‐likelihood models. The genus is divided into two well‐supported clades and two poorly supported clades at the root of the phylogeny with incomplete phylogenetic resolution within two species groups, likely due to rapid speciation. Izatha display a number of apomorphic phallic traits including cornuti (sclerotized spines) which are either discharged into the female during copulation (deciduous cornuti) or fixed to the male phallus (compound and fish‐hook cornuti). Within the genus, there is a reduction of secondary genital characters – the uncus and gnathos – but an elaboration of another grasping structure, the juxta; the potential origin and functionality of these male genital traits are discussed. Overall, some male genital characters provided a good indication of species relationships; however, several parts of the complex male genitalia of Izatha show evidence of homoplasy and convergence highlighting the problems of using these traits in determining species relationships. Additionally, this convergence has highlighted that complex genital structures may evolve repeatedly and independently within a lineage.     

Experimental modifications imply a stimulatory function for male tsetse fly genitalia,supporting cryptic female choice theory

One of the most sweeping of all patterns in morphological evolution is that animal genitalia tend to diverge more rapidly than do other structures. Abundant indirect evidence supports the cryptic female choice (CFC) explanation of this pattern, which supposes that male genitalia often function to court females during copulation; but direct experimental demonstrations of a stimulatory function have been lacking. In this study, we altered the form of two male genital structures that squeeze the female’s abdomen rhythmically in Glossina pallidipes flies. As predicted by theory, this induced CFC against the male: ovulation and sperm storage decreased, while female remating increased. Further experiments showed that these effects were due to changes in tactile stimuli received by the female from the male’s altered genitalia, and were not due to other possible changes in the males due to alteration of their genital form. Stimulation from male genital structures also induces females to permit copulation to occur. Together with previous studies of tsetse reproductive physiology, these data constitute the most complete experimental confirmation that sexual selection (probably by CFC) acts on the stimulatory properties of male genitalia.     

Body Dysmorphic Disorder: Contraindication or Ethical Justification for Female Genital Cosmetic Surgery in Adolescents

Is Female Genital Cosmetic Surgery for an adolescent with Body Dysmorphic Disorder ever ethically justified? Cosmetic genital surgery (specifically labioplasty) for adolescent girls is one of the most ethically controversial forms of cosmetic surgery and Body Dysmorphic Disorder is typically seen as a contraindication for cosmetic surgery. Two key ethical concerns are (1) that Body Dysmorphic Disorder undermines whatever capacity for autonomy the adolescent has; and (2) even if there is valid parental consent, the presence of Body Dysmorphic Disorder means that cosmetic surgery will fail in its aims. In this article, we challenge, in an evidence‐based way, the standard view that Body Dysmorphic Disorder is a contraindication for genital cosmetic surgery in adolescents. Our argument gathers together and unifies a substantial amount of disparate research in the context of an ethical argument. We focus on empirical questions about benefit and harm, because these are ethically significant. Answers to these questions affect the answer to the ethical question. We question the claim that there would be no benefit from surgery in this situation, and we consider possible harms that might be done if treatment is refused. For an adolescent with Body Dysmorphic Disorder, the most important thing may be to avoid harm. We find ourselves arguing for the ethical justifiability of cosmetic labioplasty for an adolescent with Body Dysmorphic Disorder, even though we recognize that it is a counter intuitive position. We explain how we reached our conclusion.