A Test of Genital Allometry Using Two Damselfly Species does not Produce Hypoallometric Patterns

It is widely admitted that sexual selection is the responsible force behind genital traits. However, the particular mechanisms of genital evolution are still debated. Recently, studies of genital static allometry in insects have been used to elucidate such mechanisms. Insect genital traits are often reported to show negative allometry (i.e., a slope < 1), which has generated a number of ideas on how genital traits are selected. However, many studies that have inferred selection mechanisms have omitted consideration of the function of genital traits, used unreliable indicators of body size, and only rarely included female genitalia in their analysis. We investigated whether negative allometry operates for genitalia in two damselfly species (Protoneura cara and Ischnura denticollis). Damselflies are suitable for genital allometry tests as their genital function and body size indicators (wing length and head width) are relatively well known and established. First, we show that the aedeagus is used to physically remove sperm from both sperm storage organs (bursa and spermatheca) and that wing length and head width correlate positively with other morphological traits for the two study species. Second, we estimated genital allometry by measuring aedeagal length, vaginal length, bursal volume, and spermathecal volume. Our results indicate no consistent allometric pattern. Allometry for aedeagal length and vaginal width was not the same. Thus, there was no support for a negative allometric relationship. We urge researchers investigating allometry to look directly at how genitalia function rather than inferring function from allometric relationships only.     

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.     

Sexual selection and genital allometry in the Hottentot golden mole (Amblysomus hottentotus)

Under sexual selection, genitalia typically undergo rapid and divergent evolution across species and competition between the sexes over control of fertilisation may drive the co-evolution of male and female sexual traits. Sexual selection can, therefore, influence genitalia in three fundamental but non-mutually exclusive ways: (1) cryptic female choice, (2) sperm competition and (3) sexual conflict. Golden moles (Chrysochloridae) are a highly specialised family endemic to sub-Saharan Africa. We examined intra-specific genital allometry of both male and female subterranean Hottentot golden moles (Amblysomus hottentotus). Consistent with previous studies in mammals, we found positive allometry and a high coefficient of variation (CV) for male genitalia. The results for female reproductive tract length of A. hottentotus contrast with the findings of previous studies as isometry was recorded. Based on the allometric relationships of both males and females presented here, we suggest that the males do not sequester females and that in the absence of visual cues the female may use penis size as an indicator of phenotypic quality.     

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.     

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.     

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.     

BOTH MALE AND FEMALE NOVEL TRAITS PROMOTE THE CORRELATED EVOLUTION OF GENITALIA BETWEEN THE SEXES IN AN ARTHROPOD

The correlated evolution of genitalia between sexes has been demonstrated in many taxa. However, it remains unclear whether female rather than male genitalia can play a key role in the correlated evolution of male and female genitalia. We conducted an extensive cross‐population analysis of the divergence patterns of genital structures, weights of whole genital organs, and the bodies of both sexes, and male genital length in a group of xystodesmid millipedes showing diverse genital morphologies. We demonstrate that the correlated evolution of male and female genitalia toward exaggerated states has occurred in the millipedes, which have evolved novel traits in both males (forceps‐like gonopods) and females (retractable bellows). Enlargement and elongation of forceps‐like gonopods may be advantageous in sperm competition, whereas enlargement and elongation of the bellows may facilitate acceptance/rejection of insemination for ensuring the female's fitness. These male and female genital parts have affected the correlated evolution in the opposite sex, resulting in diversification and exaggeration of genital morphology. Our study suggests that evolutionary novel traits in not only males but also in females could play an important role in the correlated evolution of genitalia between the sexes.     

Bat genitalia: allometry, variation and good genes

Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 497–507.     

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.     

Allometry in damselfly ornamental and genital traits: solving some pitfalls of allometry and sexual selection

Static allometry of sexually selected traits has been the subject of intense research recently. However, some pitfalls for this kind of research are: (a) the functions of sexual traits are largely unknown; (b) more than one body size indicator must be measured; and, (c) allometry must be examined under different environmental circumstances to see whether allometric values change. Using Hetaerina americana damselflies, we investigated the type of allometry exhibited by a wing red spot and aedeagal width. These traits are positively selected during pre-copulatory male-male contests and post-copulatory female stimulation, respectively. As body size indicators, we used wing length and head width. It has been documented that expression of both sexual traits varies throughout the year. Thus, allometry was examined in different times of the year. We also investigated the allometry of aedeagal width and vaginal width at the zone where female stimulation takes place. We found no clear pattern of any allometric relationship for male and female traits and for both body size indicators at all times sampled. Our results contrast with patterns of negative allometry exhibited by genital traits in other animals.     

No evidence for condition-dependent expression of male genitalia in the dung beetle Onthophagus taurus

We examine the condition-dependence of male genitalia in the dung beetle Onthophagus taurus by manipulating the quality of dung provided for larval growth and development. We show that the influence of larval nutrition differed considerably across three different trait classes (sexual, nonsexual and genital). The size of all nonsexual traits varied with dung quality but their allometric slopes remained unchanged. Relative horn length and allometry, but not absolute horn length, showed a high degree of plasticity with differences in dung quality. In contrast, both absolute size and allometry of genitalia were largely unresponsive to changes in dung quality. Male genitalia exhibited intermediate levels of phenotypic variation and lower allometric slopes than both horns and nonsexual traits. Thus, our findings provide little support for good genes hypotheses of genital evolution. We use our findings to discuss a developmental mechanism and selection pressures that may prevent the condition-dependent expression of genitalia.     

BACULAR AND TESTICULAR GROWTH AND ALLOMETRY IN THE CAPE FUR SEAL ARCTOCEPHALUS P. PUSILLUS (OTARIIDAE)

The baculum in Arctocephalus p. pusillus reaches up to 14.1 cm in length, 13.5 g in mass, and 1.3 g/cm in density (= mass/length). A pubertal growth spurt occurs between 2 and 3 yr of age, when bacular length increases by 28%, mass by 124%, and density by 77%; concurrently, body length increases by 14%. A second, weaker spurt occurs at social maturity (9-10 yr of age). Testes grow most rapidly between 1 and 2 yr of age, when testicular length increases by 29%. After 3 yr of age, growth in bacular and testicular length slows, and bacular mass continues to increase approximately linearly. Bacular and testicular lengths average 6.8% and 3.4% (respectively) of body length in adults, compared with 9.9% and 5.7% in the promiscuous harp seal ( Pagophilus groenlandicus ). Bacular length, mass, and density, and testicular length, are positively allometric to body length over growth; bacular length is isometric to testicular length. Among animals of the same age, bacular length and mass are positively allometric to body length in young animals, with negative allometry or isometry thereafter; testicular length is isometric to body length in young animals and negatively allometric thereafter. Patterns of early growth and allometry of the baculum and testes are interpreted as adaptations for mating opportunities, years before territoriality is possible. The baculum and testes of adult Cape fur seals and other otariids are small compared with those of most phocids, because sperm competition among male otariids is weak.     

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.     

Phenotypic and genetic variation in male genitalia in the seedbug, Lygaeus equestris (Heteroptera)

Male genitalia evolve through sexual selection and, in insects, tend to show negative static allometry, low phenotypic variation, and are usually relatively small. Much less is known about the genetic variation and heritability of male genitalia. Additionally, in instances where the intromittent organ is greatly elongated, it is unclear whether typical patterns of genital scaling and variation also apply. In the present study, we investigated the allometry, variation, and heritability of male genital length in the seedbug, Lygaeus equestris , a species with a greatly elongated intromittent organ (i.e. almost as long as male body size). We found that genital length was negatively allometric, in spite of its great length, and was no more variable than nongenital traits. Additionally, genital length was significantly heritable and had considerable evolvability.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 400–405.     

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.     

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.     

Sperm competition risk and male genital anatomy: comparative evidence for reduced duration of female sexual receptivity in primates with penile spines

Selection pressures influencing the way in which males stimulate females during copulation are not well understood. In mammals, copulatory stimulation can influence female remating behaviour, both via neuroendocrine mechanisms mediating control of sexual behaviour, and potentially also via effects of minor injury to the female genital tract. Male adaptations to increase copulatory stimulation may therefore function to reduce sperm competition risk by reducing the probability that females will remate. This hypothesis was tested using data for primates to explore relationships between male penile anatomy and the duration of female sexual receptivity. It was predicted that penile spines or relatively large bacula might function to increase copulatory stimulation and hence to reduce the duration of female sexual receptivity. Results of the comparative analyses presented show that, after control for phylogenetic effects, relatively high penile spinosity of male primates is associated with a relatively short duration of female sexual receptivity within the ovarian cycle, although no evidence was found for a similar relationship between baculum length and duration of female sexual receptivity. The findings presented suggest a new potential function for mammalian penile spines in the context of sexual selection, and add to growing evidence that sperm competition and associated sexual conflict are important selection pressures in the evolution of animal genitalia.     

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.     

Ontogeny of sexual dimorphism in the Long-tailed Manakin Chiroxiphia linearis: long maturation of display trait morphology

Males of dimorphic species often show ornaments that are thought to have evolved through female choice or/and male–male competition. The sexual differentiation of similar morphologies occurs during ontogeny, resulting in differential sex and age-specific selection. The Long-tailed Manakin is a dimorphic species with a highly skewed mating system, the males of which delay plumage maturation over 3 to 4 years. We describe ontogenetic changes in feather morphology in this species through sexual maturity. Males showed a significant increase in length of the central rectrices with age, hence their degree of sexual dimorphism increased from zero in 1-year-old males to 189.5% in adults. In contrast, male tail length decreased with age. Wing length did not vary significantly with age, but females had relatively longer wings than males. Wing loading was greater in females and decreased with age in males. In adults, rectrix length was positively correlated with testis volume, supporting the hypothesis that secondary sexual characters can signal the condition of primary sexual characters. Rectrix length showed positive allometry with body size in males less than 4 years old, whereas older males showed negative allometry and females showed isometry. Wing area and wing loading shifted from negative to positive allometry in males of 2 to 3 years of age. Changes in male morphology during ontogeny in the Long-tailed Manakin appeared to be associated with their specific display behaviours. Age-related changes in allometric growth of rectrices in the Long-tailed Manakin suggested that young males invest disproportionately more in the length of this trait relative to their body size. This investment could act as a signal of competitive ability to move status position in their orderly queue.     

Static allometry and animal genitalia

A survey of 117 species of arthropods and 17 species of vertebrates showed a strong trend for male genitalia to have relatively low static allometric values. This trend contrasts with the allometry of other structures under sexual selection, which usually show steep allometric slopes. The trend to low allometric genital values is less consistent in mammals than in arthropods. Data not in accord with the previous the "one-size-fits-all" explanation for low allometric slopes in genitalia, which was based on sexual selection by female choice, suggest a more general version that includes both natural selection and sexual selection, and involves both mechanical fit and stimulation. Less-complete data on the female genitalia of arthropods suggest a trend to similar low allometric slopes, and may also be explained by mechanical fit and stimulatory one-size-fits-all arguments.