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.     

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,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Allometry of the baculum and sexual size dimorphism in American martens and fishers (Mammalia: Mustelidae)

Genitalia are among the most variable of morphological traits, and recent research suggests that this variability may be the result of sexual selection. For example, large bacula may undergo post‐copulatory selection by females as a signal of male size and age. This should lead to positive allometry in baculum size. In addition to hyperallometry, sexually selected traits that undergo strong directional selection should exhibit high phenotypic variation. Nonetheless, in species in which pre‐copulatory selection predominates over post‐copulatory selection (such as those with male‐biased sexual size dimorphism), baculum allometry may be isometric or exhibit negative allometry. We tested this hypothesis using data collected from two highly dimorphic species of the Mustelidae, the American marten (Martes americana) and the fisher (Martes pennanti). Allometric relationships were weak, with only 4.5–10.1% of the variation in baculum length explained by body length. Because of this weak relationship, there was a large discrepancy in slope estimates derived from ordinary least squares and reduced major axis regression models. We conclude that stabilizing selection rather than sexual selection is the evolutionary force shaping variation in baculum length because allometric slopes were less than one (using the ordinary least squares regression model), a very low proportion of variance in baculum length was explained by body length, and there was low phenotypic variability in baculum length relative to other traits. We hypothesize that this pattern occurs because post‐copulatory selection plays a smaller role than pre‐copulatory selection (manifested as male‐biased sexual size dimorphism). We suggest a broader analysis of baculum allometry and sexual size dimorphism in the Mustelidae, and other taxonomic groups, coupled with a comparative analysis and with phylogenetic contrasts to test our hypothesis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 955–963.     

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.     

Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish

In 1950, Rensch noted that in clades where males are the larger sex, sexual size dimorphism (SSD) tends to be more pronounced in larger species. This fundamental allometric relationship is now known as ‘Rensch''s rule’. While most researchers attribute Rensch''s rule to sexual selection for male size, experimental evidence is lacking. Here, we suggest that ultimate hypotheses for Rensch''s rule should also apply to groups of individuals and that individual trait plasticity can be used to test those hypotheses experimentally. Specifically, we show that in the sex-changing fish Parapercis cylindrica, larger males have larger harems with larger females, and that SSD increases with harem size. Thus, sexual selection for male body size is the ultimate cause of sexual size allometry. In addition, we experimentally illustrate a positive relationship between polygyny potential and individual growth rate during sex change from female to male. Thus, sexual selection is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. Taken together, our results provide compelling evidence in support of the sexual selection hypothesis for Rensch''s rule and highlight the potential importance of individual growth modification in the shaping of morphological patterns in Nature.     

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.     

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.     

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.     

Allometry, bilateral asymmetry and sexual differences in the vocal tract of common eiders Somateria mollissima and king eiders S. spectabilis

Intraspecific sexual differences, high variation, and positive allometry of sexually-selected external display structures are common. Many sexually-selected anatomical specializations occur in the avian vocal tract but intraspecific variation and allometry have been investigated little. The tracheal bulla bulla syringealis occurs in males of most duck species. We quantified variation and size-scaling of the bulla, plus sexual differences in size of trachea, bronchi, and vocal muscles, for 62 common eiders Somateria mollissima and 51 king eiders S. spectabilis. Trends were similar in both species. Bullar ossification and definitive size occurred early in life: bullar size did not differ between first-year and older males. Bullar size did not vary more than size of other body parts (CVs of 3.4–7.0% for bullar length and breadth). Bullar size scaled to body size with negative allometry or isometry. Vocal muscles were 10–50% thicker in males than females, a much greater sexual difference than in body size (CVs of 3–6% on linear body-size variables). Vocal muscles were larger on the left side in both sexes and bilateral asymmetry was slightly more pronounced in males. Low variation and a trend towards negative allometry suggest that bullar size is under stabilizing selection; if bullar size affects vocal attributes of voice, then the latter cannot be condition-dependent. We recommend comparative research on vocal communication, vocal individuality and vocal-tract anatomy and function in eiders and other ducks.     

Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females

When males are the larger sex, a positive allometric relationship between male and female sizes is often found across populations of a single species (i.e. Rensch’s rule). This pattern is typically explained by a sexual selection pressure on males. Here, we report that the allometric relationship was negative across populations of a shell-brooding cichlid fish Lamprologus callipterus, although males are extremely larger than females. Male L. callipterus collect and defend empty snail shells in each of which a female breeds. We found that, across six populations, male and female sizes are positively correlated with not only sexual and fecundity selection indices, but also with shell sizes. Given their different reproductive behaviours, these correlations mean that males are required to be more powerful, and thus larger, to transport larger shells, while female bodies are reduced to the shell size to enable them to enter the shells. Among the three size selections (sexual selection, fecundity selection and shell size), shell size explained the allometry, suggesting that females are more strongly subject to size selection associated with shell size availability than males. However, the allometry was violated when considering an additional population where size-selection regimes of males differed from that of other populations. Therefore, sexual size allometry will be violated by body size divergence induced by multiple selection regimes.     

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.     

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.     

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.     

Sexual conflict in wing size and shape in Drosophila melanogaster

Intralocus sexual conflict occurs when opposing selection pressures operate on loci expressed in both sexes, constraining the evolution of sexual dimorphism and displacing one or both sexes from their optimum. We eliminated intralocus conflict in Drosophila melanogaster by limiting transmission of all major chromosomes to males, thereby allowing them to win the intersexual tug‐of‐war. Here, we show that this male‐limited (ML) evolution treatment led to the evolution (in both sexes) of masculinized wing morphology, body size, growth rate, wing loading, and allometry. In addition to more male‐like size and shape, ML evolution resulted in an increase in developmental stability for males. However, females expressing ML chromosomes were less developmentally stable, suggesting that being ontogenetically more male‐like was disruptive to development. We suggest that sexual selection over size and shape of the imago may therefore explain the persistence of substantial genetic variation in these characters and the ontogenetic processes underlying them.     

Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as ‘Rensch’s rule’. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male‐biased SSD increases with body size. One of the explanations for the occurrence of Rensch’s rule is the differential‐plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch’s rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male‐larger species (Paroedura picta). In this species, males exhibited larger temperature‐induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential‐plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.     

Sex-specific responses to fecundity selection in the broad-nosed pipefish

Fecundity selection, acting on traits enhancing reproductive output, is an important determinant of organismal body size. Due to a unique mode of reproduction, mating success and fecundity are positively correlated with body size in both sexes of male-pregnant Syngnathus pipefish. As male pipefish brood eggs on their tail and egg production in females occurs in their ovaries (located in the trunk region), fecundity selection is expected to affect both sexes in this species, and is predicted to act differently on body proportions of males and females during their development. Based on this hypothesis, we investigated sexual size dimorphism in body size allometry and vertebral numbers across populations of the widespread European pipefish Syngnathus typhle. Despite the absence of sex-specific differences in overall and region-specific vertebral counts, male and female pipefish differ significantly in the relative lengths of their trunk and tail regions, consistent with region-specific selection pressures in the two sexes. Male pipefish show significant growth allometry, with disproportionate growth in the brooding tail region relative to the trunk, resulting in increasingly skewed region-specific sexual size dimorphism with increasing body size, a pattern consistent across five study populations. Sex-specific differences in patterns of growth in S. typhle support the hypothesis that fecundity selection can contribute to the evolution of sexual size dimorphism.     

SEX‐SPECIFIC PATTERNS OF MORPHOLOGICAL DIVERSIFICATION: EVOLUTION OF REACTION NORMS AND STATIC ALLOMETRIES IN NERIID FLIES

The consequences of sex‐specific selection for patterns of diversification remain poorly known. Because male secondary sexual traits are typically costly to express, and both costs and benefits are likely to depend on ambient environment and individual condition, such traits may be expected to diversify via changes in reaction norms as well as the scaling of trait size with body size (static allometry). We investigated morphological diversification within two species of Australian neriid flies (Telostylinus angusticollis, Telostylinus lineolatus) by rearing larvae from several populations on larval diets varying sixfold in nutrient concentration. Mean body size varied among populations of T. angusticollis, but body size reaction norms did not vary within either species. However, we detected diversification of reaction norms for body shape in males and females within both species. Moreover, unlike females, males also diversified in static allometry slope and reaction norms for static allometry slope of sexual and nonsexual traits. Our findings reveal qualitative sex differences in patterns of morphological diversification, whereby shape–size relationships diversify extensively in males, but remain conserved in females despite extensive evolution of trait means. Our results highlight the importance of incorporating plasticity and allometry in studies of adaptation and diversification.     

Within‐season variation in sexual selection in a fish with dynamic sex roles

The strength of sexual selection may vary between species, among populations and within populations over time. While there is growing evidence that sexual selection may vary between years, less is known about variation in sexual selection within a season. Here, we investigate within‐season variation in sexual selection in male two‐spotted gobies (Gobiusculus flavescens). This marine fish experiences a seasonal change in the operational sex ratio from male‐ to female‐biased, resulting in a dramatic decrease in male mating competition over the breeding season. We therefore expected stronger sexual selection on males early in the season. We sampled nests and nest‐holding males early and late in the breeding season and used microsatellite markers to determine male mating and reproductive success. We first analysed sexual selection associated with the acquisition of nests by comparing nest‐holding males to population samples. Among nest‐holders, we calculated the potential strength of sexual selection and selection on phenotypic traits. We found remarkable within‐season variation in sexual selection. Selection on male body size related to nest acquisition changed from positive to negative over the season. The opportunity for sexual selection among nest‐holders was significantly greater early in the season rather than late in the season, partly due to more unmated males. Overall, our study documents a within‐season change in sexual selection that corresponds with a predictable change in the operational sex ratio. We suggest that many species may experience within‐season changes in sexual selection and that such dynamics are important for understanding how sexual selection operates in the wild.     

The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders

Under natural and sexual selection traits often evolve that secure paternity or maternity through self‐sacrifice to predators, rivals, offspring, or partners. Emasculation—males removing their genitals—is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm‐transferring organs — secondary genitals — (hereafter, palps), results in ‘eunuchs’. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male–male contests (better‐fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves‐off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote‐copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb‐weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: ‘pre‐maturation’, ‘mating’, and ‘post‐mating’. We use a genus‐level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co‐evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.