Natural selection and genital variation: a role for the environment,parasites and sperm ageing?

Male genitalia are more variable between species (and populations) than other organs, and are more morphologically complex in polygamous compared to monogamous species. Therefore, sexual selection has been put forward as the major explanation of genital variation and complexity, in particular cryptic female choice for male copulatory courtship. As cryptic female choice is based on differences between males it is somewhat paradoxical that there is such low within-species variation in male genitalia that they are a prime morphological identification character for animal species. Processes other than sexual selection may also lead to genitalia variation but they have recently become neglected. Here I focus on pleiotropy and natural selection and provide examples how they link genitalia morphology with genital environments. Pleiotropy appears to be important because most studies that specifically tested for pleiotropic effects on genital morphology found them. Natural selection likely favours certain genital morphology over others in various environments, as well as by reducing re-infection with sexually transmitted diseases or reducing the likelihood of fertilisation with aged sperm. Both pleiotropy and natural selection differ locally and between species so may contribute to local variation in genitalia and sometimes variation between monogamous and polygamous species. Furthermore, the multitude of genital environments will lead to a multitude of genital functions via natural selection and pleiotropy, and may also contribute to explaining the complexity of genitalia.     

The evolution of animal genitalia: distinguishing between hypotheses by single species studies

Rapid evolution of genitalia is one of the most general patterns of morphological diversification in animals. Despite its generality, the causes of this evolutionary trend remain obscure. Several alternative hypotheses have been suggested to account for the evolution of genitalia (notably the lock-and-key, pleiotropism, and sexual selection hypotheses). Here, I argue that thorough intraspecific studies are the key to gaining insight into the patterns and processes of genitalic evolution. Critical assumptions and predictions that may be used to distinguish between the different hypotheses are identified and discussed. However, current knowledge of selection on genitalia, or even of the degree of phenotypic and genotypic variability of genital morphology, is highly limited, allowing only a very tentative assessment of the various hypotheses. In-depth single species studies of current patterns and processes of selection on genitalia are badly needed, and a single species research program is briefly outlined.     

The evolution of female genitalia

Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long‐standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison with male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here, we examine evidence for three mechanisms of genital evolution in females: species isolating ‘lock‐and‐key’ evolution, cryptic female choice and sexual conflict. Lock‐and‐key genital evolution has been thought to be relatively unimportant; however, we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species; however, the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution.     

中国尾蛱蝶属雄性外生殖器比较形态学研究(鳞翅目,蛱蝶科,螯蛱蝶亚科)

对中国尾蛱蝶属Polyura9个种的雄性外生殖器进行了比较形态学研究,结果表明,雄性外生殖器种间存在明显差异,可作为种类鉴别依据;并根据雄性外生殖器特征编制了中国尾蛱蝶属的种检索表。     

Unresolved questions in genitalia coevolution: bridging taxonomy,speciation, and developmental genetics

Systematists and geneticists study biological diversity, but they use different approaches that rarely intersect. A very common pattern that is of interest for both researchers is the rapid evolution of genitalia, a trait of significant taxonomic utility in several sexually reproducing animal clades. The idea that both male and female genitalia are species-specific and play a role in reproductive isolation has long been controversial but has recently gained a renewed interest by speciation and developmental geneticists. Here, I highlight six unresolved questions in genitalia coevolution and I argue that systematists, with their well training in comparative morphology, usage of large and geographically diverse collections, and ability to apply molecular genetics techniques, can make important contributions. Such an extension of systematics into the speciation and developmental genetics realms is a promising opportunity to expand “integrative taxonomy” comparisons between DNA and morphology into more explanatory relationships between the two sources of taxonomic data.     

Phylogeny and classification of the Catantopidae at the tribal level (Orthoptera, Acridoidea)

The grasshopper family Catantopidae is a well-known group, whose members include some of the most notorious agricultural pests. The existing classifications of the family are mostly utilitarian rather than being based on phylogenetic analysis and therefore unable to provide the stability desired for such an economically important group. In the present study, we present the first comprehensive phylogenetic analysis of the family based on morphology. By extensively sampling from the Chinese fauna, we included in the present analysis multiple representatives of each of the previously recognized tribes in the family. In total, we examined 94 genera represented by 240 species and evaluated 116 characters, including 84 for external morphology and 32 for male genitalia. The final matrix consists of 86 ingroup taxa and 88 characters. Our phylogenetic analyses resulted in a high resolution of the basal relationships of the family while showed considerable uncertainty about the relationships among some crown taxa. We further evaluated the usefulness of morphological characters in phylogeny reconstruction of the catantopids by examining character fit to the shortest trees found, and contrary to previous suggestions, our results suggest that genitalia characters are not as informative as external morphology in inferring higher-level relationship. We further suggest that earlier classification systems of grasshoppers in general and Catantopidae in particular most probably consist of many groups that are not natural due the heavy reliance on genitalia features and need to be revised in the light of future phylogenetic studies. Finally, we outlined a tentative classification scheme based on the results of our phylogenetic analysis.     

The impact of culture on sex assignment and gender development in intersex patients.

The appearance of the external genitalia is the major determinant of the social sex, which is announced at or shortly after birth. In the absence of normal development of the external genitalia, definitive gender assignment and its announcement have to be postponed. While over the past 20 years the pathogenesis of most disorders causing abnormal development of the genitalia have been elucidated, our knowledge regarding the impact of these defects upon the psychosexual development is rather rudimentary. This information, however, is needed not only to establish criteria for correct sex assignment but also to design relevant outcome studies. Culture is an important part of the context in which decisions are made on sex assignment of patients with abnormalities of the external genitalia. Cultural differences in dealing with intersexuality and intersex individuals not only influences the patient's own psychosexual development but also medical decisions regarding sex assignment and consecutive management. There is evidence that attitudes concerning gender and sexuality, including the acceptance of intersexuality, differ significantly between various cultures. Thus cross-cultural studies might allow a new approach in dealing with intersexed persons, their families, and their social background, a most important aspect considering the recent discussions and criticisms of patients and individuals affected with intersex disorders.     

Size matters: genital allometry in an African mole-rat (Family: Bathyergidae)

Typically, sexually selected traits show positive allometry and high coefficients of variation (CV). To date, many studies on the allometry of genitalia have focused on insects. In addition, studies have largely ignored the potential for sexual selection on female genitalia, despite male and female structures presumably co-evolving. Insects tend to show negative allometry in both male and female genitalia, while in contrast, the few studies carried out in mammals (males only) show positive allometry. Reasons for these differences between the taxa still remain unclear. However, in mammals, three main mechanisms have been proposed for genital evolution, namely, sperm competition, female cryptic choice and sexual conflict. In the first such study that we are aware of, we examined intra-specific genital allometry in both males and females of a mammal, the subterranean solitary Cape dune mole-rat, Bathyergus suillus. We found positive allometry occurring in male genitalia, which is consistent with previous vertebrate studies. Similarly, we found that female genitalia also exhibited positive allometry further supporting the notion of co-evolution of male and female genitalia. Although it is difficult to distinguish between the forces or mechanisms determining this directional selection, we suggest that several reproductive advantages are incurred as a result of positive allometric relationship of the genitalia in B. suillus and such advantages are also likely in other subterranean mammals. Our study further highlights the differences in genital allometry across taxa.     

基于雌蚊尾器形态的中国阿蚊属分类研究

【目的】明确阿蚊Armigeres雌蚊尾器在分类鉴定中的价值。【方法】依据在云南长期采集的标本, 观察了我国阿蚊属Armigeres正式记录的16种雌蚊尾器构造, 对雌蚊尾器的形态进行了系统描述和分类研究。【结果】编制两个亚属和16种阿蚊的雌蚊尾器分类检索表。【结论】每一种雌蚊尾器与雄蚊尾器一样, 都具有种的固定的特征, 是种的重要分类依据。     

Mosaic pattern of genital divergence in three populations of Schistocerca lineata Scudder, 1899 (Orthoptera: Acrididae: Cyrtacanthacridinae)

Sexual selection theory predicts that genital structures in isolated populations are likely to diverge, but male genitalia are often species-specific, which led to the idea that male genitalia are relatively invariable within species. Previous allometric studies collectively suggested that male genitalia are intraspecifically invariable in size compared with external body parts. We investigated whether male genitalia are invariable in shape in three populations of a grasshopper Schistocerca lineata Scudder, 1899, using two independent methods of geometric morphometric analyses. Specifically, we focused on the idea that male genitalia are complex structures consisting of many functionally different components, and studied how these individual parts diverge among three populations. Individual components of male genitalia show different population-level divergence, resulting in the mosaic pattern of genital divergence. Individual components diverge independently from each other. Body size is positively correlated with genitalia size, but is significantly correlated with the shape of only one of the three genital structures we measured. Thus, different components of male genitalia may be influenced by different evolutionary processes. This study is the first to show that components of complex genitalia evolve separately within a species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 289–301.     

Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation

According to sexual cannibalism theory, male complicity in terminal mating can be adaptive when the male's future reproductive value is low relative to the benefits of self sacrifice. Spiders and insects that exhibit male sacrifice behavior (either complicity in cannibalism or spontaneous death associated with copulation) often also have male genitalia that stereotypically become broken or disfigured the first time they are used for copulation, potentially lowering his future reproductive value. Theoretical work on monogamy has identified male bias in the effective sex ratio as a precursor to the evolution of monogamy (including male sacrifice) as an adaptive form of paternity protection. Using phylogeny-based statistics and drawing on several phylogenetic studies of araneoid spiders, I investigate relationships between male sacrifice behavior, genital mutilation, extreme sexual size dimorphism, and the accumulation of multiple males in the female web (as an indicator of a male-based effective sex ratio). This investigation focuses on araneoid spiders because several independent origins of sacrifice behavior are known for this group and the phylogenetic structure of the lineage is relatively well studied. I report that male genital mutilation is significantly correlated with sacrifice behavior and argue that this finding is consistent with sexual cannibalism theory. Male sacrifice behavior is also correlated with male accumulation, a result that is consistent with theoretical work on the evolution of monogamy. Male accumulation and extreme sexual size dimorphism are correlated suggesting that sex-based differences in maturation time can lead to a male biased effective sex ratio. Similar patterns of correlated characters may hold for some insect taxa. Studying traits that have appeared independently in multiple lineages is a powerful method for developing general theories about the evolution of biological phenomena.     

Rapid differentiation and asynchronous coevolution of male and female genitalia in stink bugs

Despite claims that genitalia are among the fastest evolving phenotypes, few studies have tested this trend in a quantitative and phylogenetic framework. In systems where male and female genitalia coevolve, there is a growing effort to explore qualitative patterns of evolution and their underlying mechanisms, but the temporal aspect remains overlooked. An intriguing question is how fast male and female genitalia may change in a coevolutionary scenario. Here, we apply a series of comparative phylogenetic analyses to reveal a scenario of correlated evolution and to investigate how fast male and female external, nonhomologous and functionally integrated genitalia change in a group of stink bugs. We report three findings: the female gonocoxite 8 and the male pygophore showed a clear pattern of correlated evolution, both genitalia were estimated to evolve much faster than nongenital traits, and rates of evolution of the male genitalia were twice as fast as the female genitalia. Our results corroborate the widely held view that male genitalia evolve fast and add to the scarce evidence for rapidly evolving female genitalia. Different rates of evolution exhibited by males and females suggest either distinct forms or strengths of selection, despite their tight functional integration and coevolution. The morphological characteristics of this coevolutionary trend are more consistent with a cooperative adjustment of the genitalia, suggesting a scenario of female choice, morphological accommodation, lock‐and‐key or some combination of the three.     

Do mating strategies determine genital allometry in African mole rats (Bathyergidae)?

Allometry describes the relationship of components of an organism with change in overall body size and has become the focus of numerous studies on the evolution of genitalia. Typically, negative allometry is observed in insects and is explained by stabilizing selection whereas the very few studies on mammals have shown a positive allometric relationship of genitalia in the body size, thought to have arisen as a result of sexual selection. However, all mammal species studied to date are thought to use mainly post-copulatory mating strategies. Across mammals, however, both pre-and post-copulatory strategies occur (although the two are not mutually exclusive). We propose that where pre-copulatory strategies are mainly used, no reproductive benefits would result from evolving positively allometric genitalia. As such, mammal genitalia are not typically positively allometric but rather allometry will, to a certain degree, be determined by mating strategy. We tested this prediction using four species of African mole rats (Bathyergidae) exhibiting variation in their life histories and mating strategies. Although generally supported, in that positive allometry did not occur in species that we assumed use mainly pre-mating strategies, positive allometry did not occur in either of the promiscuous species thought to use post-copulatory strategies. We suggest, therefore, that while mating strategies may tentatively determine genital allometry, whether positively allometric genitalia occur also depends on a number of complex interacting factors. In addition, this study provides further evidence and empirical support for the co-evolution of male and female genitalia in mammals.     

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the ‘one‐size‐fits‐all’ hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One‐size‐fits‐all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One‐size‐fits‐all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.     

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.     

Female genitalia,reproductive cycle and sperm storage in Armadillidium vulgare (Crustacea,Isopoda, Oniscidea)

Light and electron microscopic studies that we have published in the past have reported many aspects of the reproductive process in Armadillidium vulgare with particular emphasis on the reconstruction of female genitalia. Together this body of work provides an almost complete, albeit fragmented picture of these processes and include many data on sperm storage and sperm translocation. Females of A. vulgare have a pair of cuticular genitalia in the lumen of the oviduct. For insemination, these genitalia can receive the copulatory organs of males formed by the elongated tips of the first two pleon endopods. During transitions between reproductive (parturial) and non-reproductive (normal, non-parturial) moult cycles the genitalia undergo intriguing structural changes resulting in two types of genitalia. Throughout their reproductive lifetime, either type is reconstructed after each moult depending on the reproductive phase of the female. In this review, we integrate the events that occur during a reproductive cycle with particular emphasis on the genitalia reconstruction and sperm storage, and discuss functional aspects of the genitalia. Thereby, we provide a case model that can be useful for further studies on genitalia diversity and female reproductive strategies in terrestrial isopods.     

中国奕刺蛾属与焰刺蛾属分类研究

属名Iragoides Hering长期被视为Phlossa Walker的同物异名,两者全世界已知12种。通过解剖我国已有的种类,发现它们的外生殖器结构并不相同,两个属的模式种各代表一个类型,因此,本文复用Iragoides Hering为有效名。奕刺蛾属Phlossa的雄性外生殖器具有刺蛾科的典型结构; 雌性外生殖器的囊导管端部多少有些呈螺旋状,囊突1枚呈新月形。奕焰刺蛾属Iragoides的雄性外生殖器在阳茎端基环两侧有膜质小突起或尾端有微刺突; 雌性外生殖器有相连的2枚囊突,囊突上有许多微齿突。共整理出中国奕刺蛾属Phlossa 4种、焰刺蛾属Iragoides 5种,后者包括1新种--线焰刺蛾I. lineofusca Wu et Fang, 及1新记录种--别焰刺蛾I. elongate Hering。编制了两个属已知种的检索表,提供了成虫彩色照片和外生殖器特征图。模式标本保存在中国科学院动物研究所。     

鳖扁蜡蝉和娇弱鳎扁蜡蝉雌性生殖器的描述(半翅目,蜡蝉总科,扁蜡蝉科)

对扁蜡蝉科(半翅目,蜡蝉总科)中鳖扁蜡蝉Cixiopsis punctatus Matsumura和娇弱鳎扁蜡蝉Tambinia debilis St(a)l的雌性生殖器进行了详细描述,绘制特征图并指明各部分的结构名称.结果表明前者生殖管道属于单开口类型,而后者是双开口类型.雌性生殖器特征可为分类学和系统发育分析提供更多的参考信息.     

Geometric morphometrics reveal male genitalia differences in the Lasiommata megera/paramegaera complex (Lepidoptera, Nymphalidae) and the lack of a predicted hybridization area in the Tuscan Archipelago

The recognition of specific demarcation between allopatric populations, as for island endemics, is particularly difficult according to the Biological Concept of Species. However, the recognition of the specific status of island taxa is decisive in evaluating important areas of endemism for conservation purposes. The recent taxonomic inflation of European butterfly species calls into question the validity and objectivity of taxonomic practices, and of databases dependent on them, which are used in biogeography and conservation. In this paper I applied rigorous morphometric analyses instead of visual evaluation to solve the long debated question of whether Lasiommata paramegaera butterfly from Sardinia and Corsica should be considered as a separated entity from the widespread Lasiommata megera . First, I carried out analyses of male genitalia shape comparing the populations from Corsica and Tuscany. Thereafter, I also searched for possible hybridization evidence in the sole area where it is strongly predicted: the Tuscan Archipelago. These islands are located between Tuscany and Corsica and there is large evidence of a continuous immigration of butterflies from these two main sources. I found that Corsican L. paramegaera and Tuscan L. megera can be clearly distinguished on the basis of genitalia shape. Furthermore, the Lasiommata population of each islet clearly maintains the characteristics of one of the two species without evidence of intermediate individuals. In conclusion, I suggest that the two entities should be considered as separate species maintaining their homogeneity by a reduced gene flow across sea, mating avoidance and/or by some depletion of F1 hybrids in developmental or mating success.     

Variation in the genitalia of the butterfly Maniola jurtina (Lepidoptera: Satyrinae)

The genilalia of animals, particularly insects, are extremely useful taxonomic characters, for they are highly conserved within species yet generally diverge rapidly during specialion: often the only reliable means of separating sibling species is via the morphology of the genilalia. A number of explanations have been proposed to explain this pattern of variation, the most prominent of which is the 'lock-and-key' hypothesis. This hypothesis and others are tested using the meadow brown butterfly, Maniola jurtina (L.), which exhibits variation in the male genitalia. A novel technique is described which enables dissection of copulating couples. Sampling and dissection of male butterflies from 14 populations in southern England was carried out to quantify variation in the genitalia. Mating success and the strength of the male-female bond during copulation was assessed in relation to the dimensions of the male genitalia.
The most variable portions of the male genitalia are the distal and dorsal margins of the paired valves. Contrary to the lock-and-key hypothesis, and the more recent sexual selection model, evidence is presented that the most variable portions of the genitalia have no apparent function during copulation, and therefore may not be subject to direct selection. I suggest that neutrality to selection was essential for the evolution of the wide variety in genital morphology currently found in the Lepidoptera.