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.     

Baculum variation and allometry in the muskrat (Ondatra zibethicus): a case for sexual selection

Sexual selection is a powerful force that influences the evolution of a variety of traits associated with female mate choice and male–male competition. Although other factors have been implicated, sexual selection may be particularly important in the evolution of the genitalia. Traits under sexual selection typically have high phenotypic variance and positive allometry relative to non-sexual traits. Here, we test the hypothesis that the baculum (os penis) of the muskrat (Ondatra zibethicus) is under sexual selection by examining phenotypic variance and allometry relative to non-sexual traits. Muskrats were sampled from Ontario, Canada, and a variety of traits measured. Measurements included baculum length and width, and three non-sexual traits (skull length, skull width, hind foot length). We used coefficient of variation (CV) and allometric slopes calculated using reduced major axis regression to test our hypotheses. Baculum traits had significantly higher CV’s relative to non-sexual traits. Baculum traits also showed positive allometry, whereas all non-sexual traits had negative allometric relationships. In addition, baculum width had higher CV’s and steeper allometric slopes than baculum length, indicating that, in muskrat, baculum width may be more influenced by sexual selection than baculum length. Positive allometry of the baculum is consistent with other examples of mammalian genitalia, but contrasts with negative allometry found in many insects. Other examples of positive allometry and high phenotypic variance of the baculum have suggested that females may use the baculum as an indicator of male quality. “Good genes” indicator traits may be particularly important in species that mate in an environmental context that prohibits female assessment of male quality. Muskrats mate aquatically, and thus females may be unable to properly assess males prior to copulation.     

Do exaggerated chelicerae function as weapons or genitalia in a long‐jawed spider? Functional allometric analysis yields an answer

From the elongated neck of the giraffe to the elaborate train of the peacock, extreme traits can result from natural or sexual selection (or both). The extreme chelicerae of the long‐jawed spiders (Tetragnatha) present a puzzle: do these exaggerated chelicerae function as weapons or genitalia? Bristowe first proposed that Tetragnatha chelicerae function as a holdfast because these spiders embrace chelicerae during mating. This hypothesis has remained untested until now. Here, we use functional allometry to examine how extreme chelicerae develop and perform in the long‐jawed spider Tetragnatha elongata. Similar to other Tetragnatha species, chelicerae were longer in adult males than in adult females. Overall, we confirm Bristowe's hypothesis: elongation only occurred in the adult stage. However, we propose that chelicerae function as more than a holdfast in T. elongata. Male chelicerae exhibited positive allometry, which suggests scaling as weapons rather than genitalia. However, fieldwork revealed that the operational sex ratio is female‐biased and both adult male–male competition and sexual cannibalism were rarely observed. Consequently, we propose that the positive allometry of male chelicerae may result from sexual selection to mechanically mesh with larger and more fecund females. Evidence for mechanical mesh includes multiple traits ranging from apophyses and grooves to guide teeth on the basal portion of the chelicerae. In contrast, we propose that chelicerae of females are analogous to the female peacock's tail: shortened by natural selection limiting the exaggeration of sexually selected traits. Indeed, females had increased foraging efficiency compared to males and exhibited negative cheliceral allometry. We discuss the implications for the evolution of elongated chelicerae in Tetragnatha.     

Structure and allometry of genitalia in males and females of a social African ground squirrel with high polygynandry

The few studies that have looked at genital allometry in mammals have typically shown a positively allometric relationship with body size and high coefficients of variation. Cryptic female choice, sexual conflict or sperm competition are mechanisms underlying genital evolution and as these are not mutually exclusive, they are often difficult to disentangle. In addition, these mechanisms are affected by both male and female social structure and/or mating strategies and, as such, pre- and post-copulatory behaviours have been shown to alter selection on genitalia. We examined genital traits and allometry in a polygynandrous and social ground squirrel Xerus inauris . We found that male testes are positively allometric and account for 1.5% of their body weight, one of the highest percentages known for sciurids. The penis, at 42.4% of head/body length, was isometric while the female reproductive tract, 22.4% head/body length, demonstrated no such relationship. Based on the allometric relationships of both males and females presented here, in conjunction with high levels of competition for females and lack of male aggression and territoriality, we suggest that sperm competition is the most likely mechanism for the evolution of the extremely large genitalia in this species.     

Pre- and Post-Copulatory Mate Selection Mechanisms in an African Dung Beetle, <Emphasis Type="Italic">Circellium bacchus</Emphasis> (Coleoptera: Scarabaeidae)

Females of most taxa mate selectively. Mate selection may be: (1) pre-copulatory, involving active female choice and male-male competition, and (2) post-copulatory, with cryptic female choice and sperm competition. Because female dung beetles (Circellium bacchus) invest heavily in parental care by ball-rolling and remaining with developing larva they are, therefore, expected to be highly selective when mating. Mate choice in this species was investigated via behavioral observations and investigations of genital allometry of both sexes, leading to conclusions about the mechanisms of, and male characteristics important in, female choice. Male–male competition seems to be crucial in mate selection of C. bacchus, although the females appeared to show no active mate choice. There is a negative allometric relationship between genital size and body size of males as predicted by the ‘one size fits all’ hypothesis (where males have genitalia that fit average-sized females). For the females, no relationship was found between genital size and body size. This might be as a result of the non-sclerotized nature of female genitalia, which may allow for greater morphological plasticity.     

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.     

Genital and body allometry in two species of noctuid moths (Lepidoptera: Noctuidae)

One‐size‐fits‐all and related hypotheses predict that static allometry slopes for male genitalia will be consistently lower than 1.0 and lower than the slopes for most other body parts (somatic traits). We examined the allometry of genitalic and somatic morphological traits in males and females of two species of noctuid moths, Spodoptera exigua (Hübner, [1808]) and Helicoverpa armigera (Hübner, [1808]). The relationship between genitalic traits and body size was generally strongly negative‐allometric in males but with no significant differences from 1.00 in females of the two species examined. However, in females, the slope of genital traits was also lower than the slopes for somatic traits. The relationship between somatic traits and the body size indicator was approximately isometric in most cases in males, except in four traits in S. exigua, in which the slopes showed slight negative allometry, and the hind tibia in H. armigera, in which the slope had positive allometry. However, in females, some somatic traits showed isometric and some other showed negative allometry in both species. The coefficients of variation (CV) for all structures in the males were low, not exceeding 10%. Genitalic traits showed significantly lower CV than somatic traits in males. In females, somatic traits showed lower CV than genitalic traits but with no significant difference in the H. armigera. Our observations of strongly negative allometry for genitalic traits in males are consistent with stabilizing selection on genital size and we suggest that male performance in interactions with females is the source of selection on male genital allometry. The difference in the degree of phenotypic variation between genitalic and somatic traits in the two studied species is attributed to the different developmental‐genetic architectures of these traits. Female genitalia showed a similar trend to the males, although the difference between genital and somatic traits was not significant in females. This finding suggests that selection is acting differently on male and female genitalia. Positive allometry of hind tibia in H. armigera may be a result of secondary sexual function.     

Evolution of male and female genitalia following release from sexual selection

Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.     

Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia

The spectacular variability that typically characterizes male genital traits has largely been attributed to the role of sexual selection. Among the evolutionary mechanisms proposed to account for this diversity, two processes in particular have generated considerable interest. On the one hand, females may exploit postcopulatory mechanisms of selection to favour males with preferred genital traits (cryptic female choice; CFC), while on the other hand females may evolve structures or behaviours that mitigate the direct costs imposed by male genitalia (sexual conflict; SC). A critical but rarely explored assumption underlying both processes is that male and female reproductive traits coevolve, either via the classic Fisherian model of preference-trait coevolution (CFC) or through sexually antagonistic selection (SC). Here, we provide evidence for this prediction in the guppy (Poecilia reticulata), a polyandrous livebearing fish in which males transfer sperm internally to females via consensual and forced matings. Our results from a paternal half-sibling breeding design reveal substantial levels of additive genetic variation underlying male genital size and morphology—two traits known to predict mating success during non-consensual matings. Our subsequent finding that physically interacting female genital traits exhibit corresponding levels of genetic (co)variation reveals the potential intersexual coevolutionary dynamics of male and female genitalia, thereby fulfilling a fundamental assumption underlying CFC and SC theory.     

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.     

Sexual selection on forelimb muscles of western grey kangaroos (Skippy was clearly a female)

Studies of sexual selection have tended to concentrate on obvious morphological dimorphisms such as crests, horns, antlers, and other physical displays or weapons; however, traits that show no obvious sexual dimorphism may nevertheless still be under sexual selection. Sexual selection theory generally predicts positive allometry for sexually selected traits. When fighting, male kangaroos use their forelimbs to clasp and hold their opponent and, standing on their tail, bring up their hind legs to kick their opponent. This action requires substantial strength and balance. We examined allometry of forelimb musculature in male and female western grey kangaroos (Macropus fuliginosus) to determine whether selection through male–male competition is associated with sex differences in muscle development. Forelimbs of males are more exaggerated than in females, with relatively greater muscle mass in males than the equivalent muscles in females. Furthermore, while muscles generally showed isometric growth in female forelimbs, every muscle demonstrated positive allometry in males. The significant positive allometry in male forelimb musculature, particularly those muscles most likely involved in male–male combat (a group of muscles involved in grasping: shoulder adduction, elbow flexion; and pulling: arm retraction, elbow flexion), clearly suggests that this musculature is subject to sexual selection. In addition to contributing to locomotion, the forelimbs of male kangaroos can also act as a signal, a weapon, and help in clasping, features that would contribute towards their importance as a sexually selected trait. Males would therefore benefit from well‐developed musculature of the arms and upper body during competition for mates. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 923–931.     

Evolutionary causes of male-biased sexual size dimorphism from a female perspective in the seed bug Togo hemipterus (Heteroptera: Lygaeidae)

Sexual size dimorphisms (SSDs) in body size are expected to evolve when selection on female and male sizes favors different optima. Many insects show female-biased SSD that is usually explained by the strong fecundity advantage of larger females. However, in some insects, males are as large as or even larger than females. The seed bug Togo hemipterus (Scott) also exhibits a male-biased SSD in body size. Many studies that have clarified the evolutionary causes of male-biased SSD have focused only on male advantages due to male–male competition. To clarify the evolutionary causes of male-biased SSD in body size, we should examine the degree of not only the sexual selection that favors larger males but also natural selection that is acting on female fecundity. The obtained results, which showed higher mating acceptance rates to larger males, implies that females prefer larger males. No significant relationship was detected between female body size and fecundity; body size effects on female fecundity were weak or undetectable. We conclude that male-biased SSD in T. hemipterus can be accounted for by a combination of sexual selection through male–male competition and female choice favoring large males, plus weak or undetectable natural selection that favors large females due to a fecundity advantage.     

Longer exaggerated male genitalia confer defensive sperm-competitive benefits in an earwig

As evidence mounts that male genitalia can affect relative fertilisation success, the role that sexual selection has played in the rapid and divergent evolution of genitalia is becoming increasingly recognized. Unfortunately, the limited functional understanding of these complex structures and their interactions with the female reproductive tract often limit interpretation regarding their evolution. Here, we address this issue using the earwig Euborellia brunneri, where both the male intromittent organ and the female spermatheca are highly exaggerated in length yet structurally simple. In a double mating design, we use the sterile male technique to study how sperm precedence patterns are affected by male genital length, male age, and the size of the male sperm storage organ, the seminal vesicle. Relative fertilisation success exhibited considerable variation around modest last-male paternity. Only an interaction between first and second male genital length affected paternity, where males gained reduced paternity when preceded by rivals with longer genitalia. Longer genitalia confer defensive benefits in sperm competition by apparently depositing ejaculate deeper in the tubular spermatheca, safe from removal by rivals. Paternity similarly depended on an interaction between the ages of both males, likely mediated by sperm traits as testes size decreased with age. Seminal vesicle size showed positive allometry but did not affect paternity; instead, greater seminal vesicle size in last males expedited oviposition. The exaggerated yet relatively simple genitalia of E. brunneri facilitate an unusually clear example of post-copulatory selection on phenotypic variation in multiple reproductive traits.     

RESEARCH PAPER: Multiple Sexual Ornamentation Signals Male Quality and Predicts Female Preference in Minnows

Sexual ornamentation often consists of multiple components. Different sexual signals may indicate different aspects of mate quality or reflect quality in different time scales. On the other hand, same signals can have a dual function and are used both in male–male competition and courtship. Many fish species are capable of rapidly altering their colouration (ephemeral colour changes), but this capability is usually ignored in sexual selection studies. Here, we used experimentally manipulated social environments to study the ephemeral colour changes in multicomponent sexual signals of male minnows (Phoxinus phoxinus) during male–male competition and female choice. We found that the dominant males courted the females more actively and had redder and/or darker skin colouration than the subordinate males. Furthermore, darkness difference between subordinate and dominant males increased in the presence of female, which suggests that the male–male competition may increase the honesty of signalling and thus facilitate female choice. In support of this hypothesis, females had a strong behavioural preference towards the more colourful males, which may indicate female choice. As colourful males often had a higher social status than paler individuals, it is possible that females base their preference on male status, not only the colouration per se. In any case, our results suggest that sexual ornamentation of male minnows may signal status, courting activity and superior quality of the males and that these signals may have a dual function in both male–male competition and female choice. Females preferred different ornamental traits (dark and red colour patterns) relatively equally, indicating that mate choice is based on multiple cues.     

Male–male competition facilitates female choice in sticklebacks

In many species, secondary sexual characteristics are used in both male–male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three-spined stickleback Gasterosteus aculeatus, male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male–male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male–male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.     

Females prefer to associate with males with longer intromittent organs in mosquitofish

Sexual selection is a major force behind the rapid evolution of male genital morphology among species. Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male''s share of paternity. Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection. Here we show that, on average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (‘gonopodium’) than males that received a greater reduction. This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time.     

Isometric patterns for male genital allometry in four damselfly species

Recent studies have found that insect genitalic traits show negative allometry, i.e., are relatively small in relation to body size. One interpretation of this is that males use their genitalia to stimulate females. Thus, given the nature of damselfly copulation in which males physically reach the rival sperm that females have stored from previous matings, male genitalic traits are not expected to show negative allometry. To test this idea, we assessed (a) the rival sperm displacement function by the mating male and (b) allometry of aedeagal length of four damselfly species (Argia anceps, Argia tezpi, Argia extranea, and Enallagma praevarum). Sperm displacement was assessed by inspecting whether the aedeagus reached the rival sperm during copulation in mating pairs for the four species. To have a standard for comparing allometric patterns, allometry of aedeagal was compared to that of two non-genital traits, tibial, and fourth abdominal segment length. In all cases, the aedeagus was found to reach the rival sperm which supports the idea that stimulation is not the mechanism for sperm displacement but physical displacement. Aedeagal length was isometric, and its slope was lower in general compared to that of tibial length and fourth abdominal segment. Given that this isometric pattern is not common for other odonate species, our interpretation of these varying aedeagal scaling patterns in this insect order is that males’ and females’ sexual interests are in conflict (males are evolving an elongated aedeagus to reach rival sperm while females are evolving unreachable sperm storage organs to prevent displacement of stored sperm). This sexual conflict scenario would favor varying scaling patterns for aedeagal length in odonates. A final interpretation is that the risk of interspecific matings in damselflies, may also explain different species-specific, aedeagal allometries.     

Do social environments affect the use of exaggerated traits in the dobsonfly Corydalus bidenticulatus?

Male–male competition is strongly affected by female presence. In insects with primitive features such as megalopterans, however, it is not known how aggressiveness is expressed in the context of female presence. Here we examined the effect of social environments on the use of secondary sexual traits in the sexual behavior of the Mexican dobsonfly Corydalus bidenticulatus (Megaloptera: Corydalidae). Males of this species have exaggerated traits such as disproportionally elongated mandibles with no dentition, which is a secondary sexual trait used in competition over female access as well as males of other Corydalus species. We investigated how male–male interactions are carried out, and the scaling relationships of sexual and non‐sexual traits. Our results show that males of C. bidenticulatus are not indiscriminately aggressive. The decision whether to fight or not is affected by their social environments: males are aggressive against other males only when the presence of a female is detected. Results also suggest that mandibles and antennae are sexually dimorphic, being exaggerated and showing positive allometry only in males. In contrast, male genitalia, a sex‐specific trait, show negative allometry.     

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male-male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male-male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid-based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male-male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.     

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.