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

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

ONE SIZE FITS ALL? RELATIONSHIPS BETWEEN THE SIZE AND DEGREE OF VARIATION IN GENITALIA AND OTHER BODY PARTS IN TWENTY SPECIES OF INSECTS AND SPIDERS

Hypotheses regarding the function of elaborate male genitalia were tested in a sample of insects and spiders by comparing their allometric values (slopes in log-log regressions on indicators of body size) with those of other body parts. Male genitalia consistently had lower slopes than other body parts. Perhaps as a consequence of this pattern, genitalic size also tended, though less consistently, to have lower coefficients of variation than did the size of other body parts. The morphological details of coupling between males and females in several species clearly indicated that selection favoring mechanical fit is not responsible for these trends. Sexual selection on male courtship structures that are brought into contact with females in precise ways may favor relatively low allometric values, in contrast to the high values seen in the other sexually selected characters (usually visual display devices) that have been studied previously, because a female's own size will influence her perception of the contact courtship devices of a male.     

Distinctive developmental variability of genital parts in the sexually dimorphic beetle, Prosopocoilus inclinatus (Coleoptera: Lucanidae)

Recent comparative studies have revealed that the rapid diversity of genitalia is closely related to sexual selection and that genital development interacts with the development of different body parts. Hypotheses about developmental stability due to selection to genital parts were tested by estimating allometric relations in a sexually dimorphic stag beetle Prosopocoilus inclinatus . All genital parts of males scaled to body size with a slope of less than 1 and all but the median lobe (male intromittent organ) showed smaller variability than other body parts. This supported the 'one-size-fits-all' hypothesis, which suggests broad copulation opportunity by males of any size with females within a population. Nevertheless, we found large variation among different genital parts in coefficients of variation and in values of the switch point where the allometric relations varied significantly. These results strongly support the view that developmental trajectories of genital traits are not necessarily integrated. Among the genitalic traits, male intromittent organ and female genitalia exhibited large variability, suggesting a high responsiveness to the selective regimes and physical interaction during copulation. This may account for rapid diversification of genital morphology, even in closely-related populations in beetle species.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 573–581.     

Interspecific body size differentiation in species assemblages of the carabid subgenus Ohomopterus in Japan

Geographic variation and interspecific differentiation in body size (body length) were analyzed for 15 species of the carabid subgenus Ohomopterus (genus Carabus; Coleoptera, Carabidae) in Japan. Local species assemblages of this subgenus consist of up to 5 species of different size classes. These beetles exhibited sexual dimorphism in body size where females are larger than males, except Carabus uenoi, in which the male and female sizes were equivalent, possibly because of the exaggerated male genitalia. In 9 of 15 species, there was a positive correlation between mean body size and annual mean temperature of habitat, representing the converse of Bergmann's rule. However, in some cases this correlation does not hold over the range of a species because of regional differences. When allopatric and sympatric populations were compared, allopatric populations of Carabus albrechti and C. japonicus had larger bodies than sympatric populations. These intraspecific differences may have resulted from character displacement. In each local assemblage with 2 or more species, there was little interspecific overlap of body size, although the body size ratio between two species with adjacent body sizes seldom showed strict constancy. The mean size ratio between 2 adjacent species in an assemblage was reduced with the number of species, whereas the size ratio of the largest to smallest species in an assemblage increased with the number of species (i.e., the expansion of body size range). These results indicate that the body size of Ohomopterus species may have evolved in response to both climatic conditions and interspecific interactions. Because each species or species group represents the same size class over the distribution range and similar-sized species are parapatric or allopatric, the interspecific segregation in body size in local assemblages may have resulted mainly from a size assortment process during colonization. Received: June 8, 2000 / Accepted: October 10, 2000     

Character displacement in giant rhinoceros beetles

I quantitatively analyzed male morphology of two closely related rhinoceros beetles species (Chalcosoma caucasus F. and Chalcosoma atlas L.) in 12 allopatric and seven sympatric locations throughout Southeast Asia. The qualitative features and the magnitude of intraspecific variation of each species were unaltered between allopatric and sympatric locations. Across allopatric locations, body size, horn size, dimorphic dimension, and genitalia size nearly completely overlapped between C. caucasus and C. atlas. Yet, in all sympatric locations, the differences between the two species in these characters were highly significant. While the enlarged difference between the two species in body size in sympatry could be attributed to habitat differentiation, that in genitalia size far exceeded what was expected from the general body-size displacement. These results indicate that morphological character displacement in sympatry was most complete in sexual organs. This may account for the process of existing species conserving themselves as integrated units by avoiding interspecific competition and enhancing reproductive isolation.     

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.     

Variation in Body Shape across Species and Populations in a Radiation of Diaptomid Copepods

Inter and intra-population variation in morphological traits, such as body size and shape, provides important insights into the ecological importance of individual natural populations. The radiation of Diaptomid species (~400 species) has apparently produced little morphological differentiation other than those in secondary sexual characteristics, suggesting sexual, rather than ecological, selection has driven speciation. This evolutionary history suggests that species, and conspecific populations, would be ecologically redundant but recent work found contrasting ecosystem effects among both species and populations. This study provides the first quantification of shape variation among species, populations, and/or sexes (beyond taxonomic illustrations and body size measurements) to gain insight into the ecological differentiation of Diaptomids. Here we quantify the shape of five Diaptomid species (family Diaptomidae) from four populations each, using morphometric landmarks on the prosome, urosome, and antennae. We partition morphological variation among species, populations, and sexes, and test for phenotype-by-environment correlations to reveal possible functional consequences of shape variation. We found that intraspecific variation was 18-35% as large as interspecific variation across all measured traits. Interspecific variation in body size and relative antennae length, the two traits showing significant sexual dimorphism, were correlated with lake size and geographic location suggesting some niche differentiation between species. Observed relationships between intraspecific morphological variation and the environment suggest that divergent selection in contrasting lakes might contribute to shape differences among local populations, but confirming this requires further analyses. Our results show that although Diaptomid species differ in their reproductive traits, they also differ in other morphological traits that might indicate ecological differences among species and populations.     

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

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

HAVE MALE AND FEMALE GENITALIA COEVOLVED? A PHYLOGENETIC ANALYSIS OF GENITALIC MORPHOLOGY AND SEXUAL SIZE DIMORPHISM IN WEB‐BUILDING SPIDERS (ARANEAE: ARANEOIDEA)

Sexual size dimorphism (SSD) can strongly influence the evolution of reproductive strategies and life history. If SSD is extreme, and other characters (e.g., genitalic size) also increase with size, then functional conflicts may arise between the sexes. Spiders offer an excellent opportunity to investigate this issue because of their wide range of SSD. By using modern phylogenetic methods with 16 species of orb-weaving spiders, we provide strong evidence for the "positive genitalic divergence" model, implying that sexual genitalic dimorphism (SGD) increases as SSD increases. This pattern is supported by an evolutionary mismatch between the absolute sizes of male and female genitalia across species. Indeed, our findings reveal a dramatic reversal from male genitalia that are up to 87x larger than female genitalia in size-monomorphic species to female genitalia that are up to 2.8x larger in extremely size-dimorphic species. We infer that divergence in SGD could limit SSD both in spiders, and potentially in other taxa as well. Further, male and female body size, as well as male and female genitalia size, are decoupled evolutionarily. Finally, we show a negative scaling (hypoallometry) of male and female genitalic morphology within sexes. Evolutionary forces specific to each sex, such as larger female size (increased fecundity) or smaller male size (enhanced mate-searching ability), may be balanced by stabilizing selection on relative genitalic size.     

Rapid shape divergences between natural and introduced populations of a horned beetle partly mirror divergences between species

Onthophagus taurus is a polyphenic beetle in which males express alternative major (horned) and minor (hornless) morphologies largely dependent on larval nutrition. O. taurus was originally limited to a Turanic-European-Mediterranean distribution, but became introduced to several exotic regions in the late 1960s. Using geometric morphometrics, we investigate the present-day morphological shape differentiation patterns among native (Italian) and introduced (Western Australian and Eastern US) populations. We then contrast these divergences to those observed between native O. taurus and its sympatric sister species O. illyricus. Our analysis failed to find significant divergences between O. taurus populations in external morphological traits (head, pronotum) when analyses were conducted separately for each sex. However, when sexes and male morphs were analyzed together, three important differences among populations emerged. First, relative warp analyses showed that native and introduced populations diverged in certain shape components that normally distinguish major and minor male morphs. Second, comparison of covariation of body regions (head vs. pronotum) in the three populations showed that populations diverged in the nature of this covariation, suggesting that different body regions are not totally constrained to evolve in concert. Lastly, and most importantly, the analysis of genitalic shape revealed little to no divergence of female genitalia, but unexpected substantial differentiation of male genitalia among the three O. taurus populations. This suggests that genitalic shape divergence can occur extremely rapidly even in the absence of sympatry and possible reinforcement, and that the genitalia of males and females may diverge independent of one another, at least during the early stage of interpopulational divergence. Interpopulation divergences in O. taurus mirrored aspects of interspecific divergences between O. taurus and O. illyricus in some cases but not others.     

Geographical variation and diversification in the flightless leaf beetles of the Chrysolina angusticollis species complex (Chrysomelidae, Coleoptera) in northern Japan

Geographical variation and differentiation of flightless leaf beetles of the Chrysolina angusticollis species complex were analysed. Nine morphological groups were recognized on the basis of metric characters relating to body size, shape of hind wing and shape of male genitalia, and binary characters relating to females' elytral surface and larval pubescence. The nine groups were essentially parapatric or allopatric to each other. Five groups occupied a continuous geographical range each, whereas another four groups were disjunctively distributed. Morphometric distance and geographical distance between populations were significantly correlated. Analyses based on 13 allozyme loci demonstrated that six out of the nine morphological groups were further divided into more than one genetically distinct group each. Genetic similarity between populations was significantly correlated with morphometric similarity and geographical closeness. Disjunctively distributed populations of a single morphological group more often resembled geographically adjacent populations of different morphological groups than geographically remote populations of the same group. In a morphological group that occupied a wide continuous range, remote populations substantially differed genetically from each other. The results suggest that there exist at least 19 morphologically and/or genetically differentiated units in the C. angusticollis complex in northern Japan. The C. angusticollis complex is likely a superspecies composed of a number of semispecies. We postulate that the diversification of this species complex might have resulted from the repeated range contraction and expansion during the ice ages. Movement of tension zones that separate two adjacent forms might contribute to enhance their geographical differentiation.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 557–578.     

Historical divergence of mechanical isolation agents in the ground beetle Carabus arrowianus as revealed by phylogeographical analyses

In the carabid genus Carabus subgenus Ohomopterus , diverged body size and genital morphology serve as mechanical reproductive barriers. To elucidate the diverging process of body and genital sizes in Carabus arrowianus , which exhibits marked morphological diversity among geographical populations and may represent an early stage of speciation, we analysed a mitochondrial gene sequence for 1051 individuals from 63 populations and male morphology for 359 individuals from 47 populations. Two discrete morphological groups segregated by geographical barriers were distinguished, one of which possessed smaller bodies and shorter genitalia ( S group) than the other ( L group), which exhibited larger bodies and exaggerated genitalia. Genetic divergence between the two groups was significant but not large. Phylogeographical and population genetic analyses indicated that the L group was derived from the S group, and a coalescent simulation revealed that the two groups diverged during the latest middle Pleistocene (0.13 million years ago), with a much larger effective population size in the L group than the S group. Because the body size divergence could not be explained by adaptation to climatic conditions and genital morphology is considered to be subject to sexual selection, we postulated that a population division and colonization in favourable habitats caused by the Pleistocene climatic and geographical change might facilitate natural and sexual selection for enlarged body and genital sizes in the L group.     

Trade-offs during the development of primary and secondary sexual traits in a horned beetle

Resource allocation trade-offs during development affect the final sizes of adult structures and have the potential to constrain the types and magnitude of evolutionary change that developmental processes can accommodate. Such trade-offs can arise when two or more body parts compete for a limited pool of resources to sustain their growth and differentiation. Recent studies on several holometabolous insects suggest that resource allocation trade-offs may be most pronounced in tissues that grow physically close to each other. Here we examine the nature and magnitude of developmental trade-offs between two very distant body parts: head horns and genitalia of males of the horned scarab beetle Onthophagus taurus. Both structures develop from imaginal disklike tissues that undergo explosive growth during late larval development but differ in exactly when they initiate their growth. We experimentally ablated the precursor cells that normally give rise to male genitalia at several time points during late larval development and examined the degree of horn development in these males compared to that of untreated and sham-operated control males. We found that experimental males developed disproportionately larger horns. Horn overexpression was weakest in response to early ablation and most pronounced in males whose genital disks were ablated just before larvae entered the prepupal stage. Our results suggest that even distant body parts may rely on a common resource pool to sustain their growth and that the relative timing of growth may play an important role in determining whether, and how severely, growing organs will affect each other during development. We use our findings to discuss the physiological causes and evolutionary consequences of resource allocation trade-offs.     

Population variation in sexual selection and its effect on size allometry in two dung fly species with contrasting sexual size dimorphism

Body size is one of the most important quantitative traits under evolutionary scrutiny. Sexual size dimorphism (SSD) in a given species is expected to result if opposing selection forces equilibrate differently in both sexes. We document variation in the intensity of sexual and fecundity selection, male and female body size, and thus SSD among 31 and 27 populations of the two dung fly species, Scathophaga stercoraria and Sepsis cynipsea, across Switzerland. Whereas in S. cynipsea females are larger, the SSD is reversed in S. stercoraria. We comprehensively evaluated Fairbairn and Preziosi's (1994) general, three-tiered scenario, hypothesizing that sexual selection for large male size is the major driving force of SSD allometry within these two species. Sexual selection intensity on male size in the yellow dung fly, S. stercoraria, was overall positive, greater, and more variable among populations than fecundity selection on females. Also, sexual selection intensity in a given population correlated positively with mean male body size of that population for both the field-caught fathers and their laboratory-reared sons, indicating a response to selection. In S. cvnipsea, sexual selection intensity on males was lower overall and significantly positive, about equal in magnitude, but more variable than fecundity selection on females. However, there was no correlation between the intensity of sexual selection and mean male body size among populations. In both species, the laboratory-reared offspring indicate genetic differentiation among populations in body size. Despite fulfillment of all key prerequisites, at least in S. stercoraria, we did not find hypoallometry for SSD (Rensch's rule, i.e., greater evolutionary divergence in male size than female size) for the field-caught parents or the laboratory-reared offspring: Female size was isometric to male size in both species. We conclude that S. cynipsea does not fit some major requirements of Fairbairn and Preziosi's (1994) scenario, whereas for S. stercoraria we found partial support for it. Failure to support Rensch's rule within the latter species may be due to phylogenetic or other constraints, power limitations, erroneous estimates of sexual selection, insufficient genetic isolation of populations, or sex differences in viability selection against large size.     

Genotype × environment interaction in the allometry of body,genitalia and signal traits in Enchenopa treehoppers (Hemiptera: Membracidae)

Developmental plasticity may promote divergence by exposing genetic variation to selection in novel ways in new environments. We tested for this effect in the static allometry (i.e. scaling on body size) of traits in advertisement signals, body and genitalia. We used a member of the Enchenopa binotata species complex of treehoppers – a clade of plant‐feeding insects in which speciation is associated with colonization of novel environments involving marked divergence in signals, subtle divergence in body size and shape, and no apparent divergence in genitalia. We found no change in mean allometric slopes across environments, but substantial genetic variation and genotype × environment interaction (G × E) in allometry. The allometry of signal traits showed the most genetic variation and G × E, and that of genitalia showed the weakest G × E. Our findings suggest that colonizing novel environments may have stronger diversifying consequences for signal allometry than for genitalia allometry. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 187–196.     

Genital variation in a dimorphic moth Selenia tetralunaria (Lepidoptera, Geometridae)

Insect genitals vary greatly among species and provide a key tool for species-level taxonomy. Insects differing in the genitalia are often treated as discrete, reproductively isolated species. This principle dates back to the lock-and-key hypothesis, which states that genitalia vary between species in order to provide a mechanical reproductive isolation system. Thus, the hypothesis assumes low within-species variability in genital traits. However, recent studies suggest that sexual selection may be responsible for the evolution of insect genitalia. We studied allometry and genital size and shape variation in a dimorphic moth Selenia tetralunaria . We found that the genitalia showed negative allometry in relation to body size as reported in many insect and spider species. This allometry was stronger in internal genital structures than it was in external genitalia. We also found that there was more variation in internal compared with external genitalia. Finally, we found that the shape of genital structures differed between morphs in all three examined areas. S. tetralunaria is among the first reported cases of genitally dimorphic insect species. Considerable variation in internal genitalia and especially the presence of genital shape differences between morphs were not consistent with the predictions of the lock-and-key hypothesis.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 297–307.     

Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae)

The processes affecting species diversification may also exert an influence on patterns of genetic variability within species. We evaluated the contributions of five variables potentially influencing clade diversification (body size, reproductive mode, range size, microhabitat and skin texture) on mtDNA divergence and polymorphism among populations of 40 species of frogs (Mantellidae) from two rainforest communities in Madagascar. We report an inverse association between body size and nucleotide divergence between populations but find no influence of other variables on genetic variation. Body size explained ca. 11% of the variation in nucleotide divergence between populations and was coupled with high F_ST levels and an absence of haplotype sharing in small‐bodied and medium‐sized frogs. Low dispersal ability is likely the proximate mechanism producing higher population differentiation in small mantellids. The lack of genetic cohesion among populations establishes regional genetic fragmentation which in turn has the potential to accelerate rates of allopatric speciation in small frogs relative to large species. However, there is little evidence of increased speciation rates in these or other small‐bodied organisms. We reconcile these contradictory observations by suggesting that lower dispersal ability also curbs colonization of new areas, decelerating diversification in weak dispersers. Our results imply that the intermediate dispersal model also applies to amphibians and may explain inconsistent previous results on the correlation of body size and speciation rate.     

Variation of distal genitalia in the simultaneously hermaphroditic land snail Arianta arbustorum (Pulmonata,Stylommatophora) caused by sexual selection?

The most likely explanation for genitalic extravagance may be sexual selection acting either before, during, or after copulation. In promiscuous species, the intensity of postulating sexual selection may be a function of population density. In this study we examined the variability of the distal genitalia involved in spcrmatophore production, reception and manipulation of 113 adult individuals of the simultaneously hermaphroditic land snail Arianta arbustorum (L.) from six natural populations in the Eastern Alps (Gesause, Austria). We investigated the hypothesis that these genitalia increase in relation to shell size with increasing population density (range: 0.9 to 39.8 individuals/m²) and expected a higher variance of the genitalia compared to shell dimensions due to sexual selection. Genitalic size was unexpectedly inversely related to population density, probably due to increased inhibitor)^- effects of snail mucus. Patterns of variation of female and male characters did not differ. Coefficients of variation of the genitalia were significantly higher than those of the shell dimensions as predicted. This was due to a higher dispersion around the regression lines rather than higher allometric values. However, the influence of sexual selection on genitalic size and variance cannot be unambiguously determined. We discuss different scenarios emphasizing the importance of sexual selection to differing degrees and conclude that sexual selection has probably played only a minor role.     

Rapid diversification of male genitalia and mating strategies in Ohomopterus ground beetles

We analysed evolutionary diversification and covariation in male genitalia and four mating traits related to sexual selection, i.e. testis size, spermatophore size, copulation duration and post-copulatory guarding duration, in Ohomopterus ground beetles using phylogenetically independent contrasts. Male genital size and mating duration have evolved more rapidly than body size and the other traits studied. Male genital size was negatively correlated with copulation duration, suggesting that elongated male genitalia may enable decreased time investment in a single copulation because it is more effective at facilitating spermatophore deposition. Male genital size was positively correlated with spermatophore size, suggesting coevolution between offensive and defensive male mating tactics because the elongated male genitalia may be advantageous in displacement of rivals' plug-like spermatophores, and decreased mating duration may intensify sperm competition. Thus, the remarkable diversity of male genitalia in Ohomopterus may have been facilitated by the interplay between inter- and intrasexual selection processes.     

Copulatory function and development shape modular architecture of genitalia differently in males and females

Genitalia are multitasking structures whose development is mediated by numerous regulatory pathways. This multifactorial nature provides an avenue for multiple sources of selection. As a result, genitalia tend to evolve as modular systems comprising semi-independent subsets of structures, yet the processes that give rise to those patterns are still poorly understood. Here, we ask what are the relative roles of development and function in shaping modular patterns of genitalia within populations and across species of stink-bugs. We found that male genitalia are less integrated, more modular, and primarily shaped by functional demands. In contrast, females show higher integration, lower modularity, and a predominant role of developmental processes. Further, interactions among parts of each sex are more determinant to modularity than those between the sexes, and patterns of modularity are equivalent between and within species. Our results strongly indicate that genitalia have been subjected to sex-specific selection, although male and female genitalia are homologous and functionally associated. Moreover, modular patterns are seemingly constant in the evolutionary history of stink-bugs, suggesting a scenario of multivariate stabilizing selection within each sex. Our study demonstrates that interactions among genital parts of the same sex may be more fundamental to genital evolution than previously thought.