Hairstreak butterflies (Lepidoptera,Lycaenidae) and evolution of their male secondary sexual organs

Hairstreak butterflies in the Atlides Section of the Eumaeini are biologically notable for a diverse array of male secondary sexual organs. A “species recognition” hypothesis postulates that females use these organs to choose between conspecific and non-conspecific males, thereby promoting reproductive isolation. Alternately, a “sexual selection” hypothesis posits that females use these organs to choose among conspecific males. These hypotheses need not be mutually exclusive but make different predictions about the evolutionary gain and loss of male secondary sexual organs. We analysed most of the Atlides Section (Theclinae, Eumaeini) phylogenetically. Sister lineages were sympatric at 22 of 37 nodes. Nine evolutionary gains occurred in lineages that were sympatric with their phylogenetic sister, and one occurred in a lineage that was allopatric/parapatric with its sister. By contrast, seven of ten evolutionary losses occurred in lineages that were allopatric/parapatric with their sisters. These results are significantly different from those predicted by a sexual selection hypothesis. We conclude that male secondary sexual organs in the Atlides Section function primarily for species recognition and thereby promote sympatric diversification.     

Dimorphic male midshipman fish: reduced sexual selection or sexual selection for reduced characters?

In most taxa with male dimorphisms, some males are large inbody size with exaggerated secondary sexual characters (exaggeratedmorph), whereas other males in the same population are smalland have reduced secondary sexual characters (reduced morph).What selective pressures cause male dimorphisms? Reduced morphologiesmay result when a) some males develop a morphology that, inthe absence of sexual selection pressures for an exaggeratedmorphology, reduces energetic and developmental costs and/orb) some males opt for an alternative morphology that does wellat an alternative behavioral tactic such as cuckoldry. The 2mechanisms could act together, but each alone is theoreticallysufficient to drive dimorphisms. Here, we tested hypothesis"b" (sexual selection for reduced characters) in the plainfinmidshipman fish, Porichthys notatus. Behavioral plasticity betweenterritoriality and cuckoldry in an exaggerated male morph (typeI) allows for a direct comparison of cuckoldry by exaggeratedmorph males to cuckoldry by reduced morph (type II) males. Comparedwith type I cuckolders, type II cuckolders were able to remainnear the nest for longer periods before being chased by theterritorial type I male, suggesting that the reduced type IImorphology allows type II males to prolong the time before attackby territorial males. Combined with other studies showing arole of sexual selection in maintaining the exaggerated morph,the data support the "sexual selection for reduced characters"hypothesis and elucidate how sexual selection can act in differentways on different males to maintain 2 male morphologies withina single species.     

Secondary pollen presentation and the temporal dynamics of stylar hair retraction and style elongation in Campanula trachelium (Campanulaceae)

To increase the accuracy of pollen capture and transfer by pollinators some plant species have developed secondary pollen presentation structures. Because the presence of secondary pollen presentation structures at the pistil may reduce the spatial separation between the sexual functions and increase the risk of self‐interference and selfing, temporal segregation of the sexual organs, triggered by visiting insects, can be expected to occur. We investigated secondary pollen presentation and the temporal dynamics of the sexual phases in combination with the physiological self‐incompatibility system in Campanula trachelium, a protandrous insect‐pollinated herb. Stylar hair retraction (male function) and curling of the stigmatic lobes (female function) were modelled using Gompertz growth functions. Finally, we performed pollination experiments in the lab and field to assess seed set and pollen limitation under natural conditions. About 68% of the total pollen load was captured by stylar hairs. Manual manipulation of the stylar hairs, mimicking pollinator visitation, significantly shortened the male phase and accelerated the female phase, resulting in a significant decline in temporal overlap between the two sexual functions. Conversely, when pollinators and/or manual manipulations were lacking, the male phase was substantially prolonged and sexual overlap was maximal. This suggests that spreading of the sexual phases and thus the risk of sexual interference are largely determined by the interaction between stylar hairs and visiting pollinators. Natural seed set was high and not pollinator limited. Overall, these results indicate that secondary pollen presentation and partial protandry resulted in efficient pollen capture, transfer and deposition.     

Alternative male reproductive strategies in the peacock blenny

A 4-year study (1989–1992) of a population of Lipophrys pavo living in a brackish lagoon (Maugio, France) revealed three types of male during the spawning season (April to September): (i) nest-breeder males which are territorial, and have well-developed secondary sexual characteristics; (ii) non-functional males which were abundant only in 1991 when population density was very high and (iii) 1-year-old kleptogamic males with small body size which possess neither secondary sexual organs nor a testicular gland, although their testes are functional and hyperdeveloped (up to 10.5% of carcass weight). The percentage of kleptogamic males was fairly stable in the population (from 7.9 to 10.0%) and highly variable in their age class (from 8.5 to 51.3%). It is suggested that kleptogamy is a conditional strategy adopted by smaller males.     

The evolution of gender-biased nectar production in hermaphroditic plants

The evolution of secondary sexual floral traits may be driven by selection through male or female reproductive success. Even so, the gender-biased function of a floral trait is often unapparent because secondary sexual traits and primary sexual organs of both genders co-occur within most bisexual flowers. Within dichogamous plants, however, secondary sexual traits may be unambiguously expressed in association with the primary sexual organs of one gender, making these species uniquely suited to studies of natural and sexual selection on floral traits. The objectives of this article are to summarize patterns of gender-biased nectar production and to critically explore theories relevant to its evolution. We list 41 species with gender-biased nectar production and provide two sets of adaptive hypotheses for the trait: sexual selection hypotheses and inbreeding avoidance hypotheses. We formulate these hypotheses using sexual selection theory in plants and the literature that relates pollinator foraging to plant inbreeding. We also consider explanations based on resource trade-offs, enemies, and genetic correlations. Support for the sexual selection and inbreeding avoidance hypotheses is provided by only a few well-studied species. We outline a series of experiments that should facilitate sorting among hypotheses. Plants with gender-biased nectar production are likely to provide unique insights into the roles of natural and sexual selection in the evolution of floral traits.     

Host-parasitoid associations of Strepsiptera: Anatomical and developmental consequences

The strepsipteran host-parasitoid system is complex and unique, due to total dependence of the parasitoid on a living host for its survival. As a result of this, the eggs of stylopised Segestidea novaeguineae (Brancsik) (Orthoptera : Tettigoniidae) are severely deformed and have a bulbous protrusion. The structure of the chorion of the eggs in stylopised and unstylopised hosts was studied and is described. The moulting sequence in the endoparasitic, female Stichotrema dallatorreanum Hofeneder, the outer layers of the germ cells in the female strepsipteran, and the ultrastructure of the rickettsia-like microorganisms, found mainly in the female Strepsiptera, are discussed.     

Individual and synergistic effects of male external genital traits in sexual selection

Male genital traits exhibit extraordinary interspecific phenotypic variation. This remarkable and general evolutionary trend is widely considered to be the result of sexual selection. However, we still do not have a good understanding of whether or how individual genital traits function in different competitive arenas (episodes of sexual selection), or how different genital traits may interact to influence competitive outcomes. Here, we use an experimental approach based on high‐precision laser phenotypic engineering to address these outstanding questions, focusing on three distinct sets of micron‐scale external (nonintromittent) genital spines in male Drosophila kikkawai Burla (Diptera: Drosophilidae). Elimination of the large pair of spines on the male secondary claspers sharply reduced male ability to copulate, yet elimination of the other sets of spines on the primary and secondary claspers had no significant effects on copulation probability. Intriguingly, both the large spines on the secondary claspers and the cluster of spines on the primary claspers were found to independently promote male competitive fertilization success. Moreover, when large and small secondary clasper spines were simultaneously shortened in individual males, these males suffered greater reductions in fertilization success relative to males whose traits were altered individually, providing evidence for synergistic effects of external genital traits on fertilization success. Overall, the results are significant in demonstrating that a given genital trait (the large spines on the secondary claspers) can function in different episodes of sexual selection, and distinct genital traits may interact in sexual selection. The results offer an important contribution to evolutionary biology by demonstrating an understudied selective mechanism, operating via subtle trait interactions in a post‐insemination context, by which genital traits may be co‐evolving.     

Male-biased nectar production in a protandrous herb matches predictions of sexual selection theory in plants

Nectar production may disproportionately benefit male relative to female pollination success. In such cases, sexual selection is often suggested as the cause of asymmetric benefits, yet sexual selection in plants-particularly plants with hermaphroditic flowers-is infrequently tested empirically. Here, I used a protandrous herb with male-biased nectar production (Chrysothemis friedrichsthaliana, Gesneriaceae) to test predictions from sexual selection theory. During three flowering seasons, I measured nectar production, pollinator visits, and male and female fecundity following different numbers of cross-pollination events. In accordance with sexual selection predictions, (1) nectar production was greater during the male phase by at least 65%; (2) visits by the main pollinator (hummingbird Phaethornis striigularis) were limiting for part of the season, indicating that plants had to compete for pollinator visits; (3) pollinators spent 53% more time per visit and made 86% more visits to male- vs. female-phase flowers, suggesting that nectar increased male more than female pollination success; and (4) female fecundity was maximized by one visit, whereas male fecundity continued to increase with additional visits. Autonomous self-pollination further reduced visit requirements for maximum female seed set. These findings match specific sexual selection predictions: they link an observable male bias in a secondary sexual trait (nectar) to positive responses of mating participants (pollinators), resulting in more mating opportunities for mate-limited males, relative to apparently resource-limited females. This field-testing of theoretical predictions provides unique evidence that sexual selection helps maintain nectar production patterns in this and, quite likely, other hermaphroditic plant species.     

Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket <Emphasis Type="Italic">Poecilimon intermedius</Emphasis>

Unisexual reproduction is a widespread phenomenon in invertebrates and lower vertebrates. If a former sexual reproducing species becomes parthenogenetic, we expect traits that were subject to sexual selection to diminish. The bushcricket Poecilimon intermedius is one of the few insect species with obligate but diploid parthenogenetic reproduction. We contrasted characters that are involved in mating in a sexually sibling species with the identical structures in the parthenogenetic P. intermedius. Central for sexual communication are male songs, while receptive females approach the males phonotactically. Compared to its sister-species P. ampliatus, the morphology of the hearing organs (acoustic spiracle, crista acustica) and the function of hearing (acoustic threshold) are reduced in P. intermedius. Nonetheless, hearing is clearly maintained in the parthenogenetic females. Natural selection by acoustic hunting bats, pleiotropy or a developmental trap may explain the well maintained hearing function.     

Reproductive systems of the North Indian langur (Presbytis entellus entellus Dufresne)

The gross anatomy and histology of the gonads and accessory sex organs are described for male and female Presbytis e. entellus. The langur differs from other catarrhine monkeys in certain specialised characters. The “sexual skin” is not comparable to the true sexual skin of the Cercopithecinae which exhibits cyclical change during the various phases of reproduction; it is nevertheless fully developed in the adult male and serves as one of the secondary sexual characters. Certain aspects of the reproductive system strikingly resemble those of man. The combined testicular weight (0.07% body weight) is similar to the human (0.08%), and the male has ampullary glands. The cervical canal is straight like that of a baboon or man. The corpus luteum (except in the lactating female) is a hollow glandular structure. Extensive hemorrhage which always accompanies ovulation in the langur, does not appear to be a common phenomenon in any other catarrhine for which ovulation and the development of corpus luteum have been studied. The hemorrhagic remains are retained for a long time in the ovulated follicle. The ovary is characteristically large and averages 0.74 gm without corpus luteum and 1.57 gm with corpus luteum, a feature never reported in any other catarrhine monkeys. The pre-ovulatory follicle may attain a size of 14 × 14 mm.     

Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: implications for understanding developmental arrest

There are two morphs of reproductive male in orangutans. Both morphs span the age range from adolescent to adult, but "subadult" males are smaller in size and lack secondary sexual features. In this study, urine samples were collected over a 2 year period from 23 captive male orangutans in order to define the endocrinology of this apparent arrest of secondary sexual development. Three males were juveniles, 3 to 5 years of age; seven males showed no secondary sexual trait development and were over 7 years of age; six males were in the process of developing secondary sexual features, with the youngest male being 6 years of age; and seven males were fully mature adults. Morning samples were analyzed by radioimmunoassay for levels of growth hormone (GH) and thyroid-stimulating hormone (TSH) and group hormone profiles were compared by analysis of variance. GH is the primary hormone of growth and development and its increase in teenage boys is associated with the adolescent growth spurt. TSH stimulates the thyroid to produce and secrete hormones that have metabolic effects and required for normal growth and development. Results show that arrested adolescent male orangutans have a GH level about 1/3 that of developing adolescents (P = .0006). TSH levels do not differ significantly between arrested and developing adolescents. These data complement other endocrine data showing significantly lower levels of sex steroids and luteinizing hormone (LH) in arrested males than developing males [Maggioncalda, 1995a,b; Maggioncalda et al., 1999]. Together with documented behavioral differences between reproductive males with and without secondary sexual features, these endocrine data support the hypothesis that in male orangutans there are alternative developmental pathways and corresponding alternative reproductive strategies.     

The postnatal ontogeny of the sexually dimorphic vocal apparatus in goitred gazelles (Gazella subgutturosa)

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male‐specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age‐classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade‐off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826–844, 2016. © 2016 Wiley Periodicals, Inc.     

Different on the inside: extreme swimbladder sexual dimorphism in the South Asian torrent minnows

The swimbladder plays an important role in buoyancy regulation but is typically reduced or even absent in benthic freshwater fishes that inhabit fast flowing water. Here, we document, for the first time, a remarkable example of swimbladder sexual dimorphism in the highly rheophilic South Asian torrent minnows (Psilorhynchus). The male swimbladder is not only much larger than that of the female (up to five times the diameter and up to 98 times the volume in some cases), but is also structurally more complex, with multiple internal septa dividing it into smaller chambers. Males also exhibit a strange organ of unknown function or homology in association with the swimbladder that is absent in females. Extreme sexual dimorphism of non-gonadal internal organs is rare among vertebrates and the swimbladder sexual dimorphisms that we describe for Psilorhynchus are unique among fishes.     

The evolutionary significance of sexual selection

A model for the joint evolution of a secondary sexual male trait Z and a female mating preference Y is discussed. Recurrence relations for the moments of (Z, Y) are given under the assumption that the traits are binormally distributed. It is shown that female preference for a male character can lead to an equilibrium distribution of the male trait with non-zero variances. The conditions under which the distribution is stable, are given. Unstable situations, in which a continued exaggeration of the male trait occurs, are described. It is demonstrated that the effect of sexual selection on the evolution of the male trait depends on the intensity of natural selection, i.e. the effect of the sexual selection increases when the intensity of natural selection is reduced. The effect of the female preference on the male trait also increases with increasing availability of males. This provides a link to several ecological conditions which have generally been known to be correlated with the degree of sexual selection. Furthermore, it is demonstrated that perturbations away from the equilibrium may cause rapid evolution of the male character, eventually leading to speciation.     

Female Attraction to Higher Pitched Male Enticement Calls in Barn Swallows

Current sexual selection studies demonstrate that female mate preference almost always favors exaggerated male traits, such as colorful plumage and elongated tails. However, such studies focused mainly on secondary sexual characteristics, i.e., traits that are fully developed at maturation, while ignoring others, which precludes generalization of the findings. We studied the expression of the male enticement call, a nestling‐like courtship trait, in relation to female attraction and to the expression of secondary sexual ornaments in the Japanese barn swallow Hirundo rustica gutturalis. First, we showed that the peak amplitude frequency of male enticement calls was, on average, lower than that of nestling food‐begging calls, indicating that higher pitched calls are more similar to nestling food‐begging calls than are lower pitched calls. Second, we conducted an experimental playback of male enticement calls during the courtship period with the female's mate removed, and found that females were more attracted to heightened‐pitch calls than to control calls. Lastly, the peak amplitude frequency of male enticement calls was negatively related to the ornamentation, as measured by throat coloration. Taken together, these findings suggest the following: (1) females are attracted to a more nestling‐like trait, and (2) similarity to nestling food‐begging calls increases with decreasing secondary sexual ornaments. Nestling‐like male traits that are not secondary sexual characteristics should be considered when studying the general pattern of female attraction to male traits.     

Male secondary sexual traits are hydrodynamic devices for enhancing swimming performance in a monogamous filefish Paramonacanthus japonicus

The Japanese filefish Paramonacanthus japonicus has extreme sexual dimorphism in its overall shape, even though its mating system is monogamy with biparental care. This sexual dimorphism is mainly due to the development of secondary sexual traits in males. Males become more slender in body with elevated soft dorsal and anal fins as they mature. We examined the function of such male secondary sexual traits by field research and fluid-dynamic analysis. Underwater observations showed that movement rate and steady swimming speed of males were higher than those of females. Male and female P. japonicus showed similar feeding habits and egg-tending behavior, although males attacked potential egg predators more frequently. A wind-tunnel experiment using the air bearing and spring system showed that the drag coefficient of males was significantly lower than that of females, indicating a lower male hydrodynamic drag performance. Also, male elevated soft dorsal and anal fins are considered to give rise to higher thrust performance in monacanthids. Thus, these results suggest that male secondary sexual traits are hydrodynamic devices for enhancing swimming performance that seem to be actually functional under natural conditions. We discuss the evolution of such conspicuous male sexual traits in P. japonicus. Electronic Publication     

The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of mate quality because the hormones (e.g. testosterone) needed to develop secondary sexual traits have immunosuppressive effects. The best support for predictions arising from the immunocompetence handicap hypothesis so far comes from studies of insects, although they lack male-specific hormones such as testosterone. In our previous studies, we found that female mealworm beetles prefer pheromones of immunocompetent males. Here, we tested how juvenile hormone (JH) affects male investment in secondary sexual characteristics and immune functions in the mealworm beetle, Tenebrio molitor. We injected male mealworm beetles with JH (type III) and found that injection increased the attractiveness of male pheromones but simultaneously suppressed immune functions (phenoloxidase activity and encapsulation). Our results suggest that JH, which is involved in the control of reproduction and morphogenesis, also plays a central role in the regulation of a trade-off between the immune system and sexual advertisement in insects. Thus, the results reflect a general mechanism by which the immunocompetence handicap hypothesis may work in insects.     

Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx)

Male mandrills (Mandrillus sphinx) have spectacular secondary sexual adornments. These include red and blue sexual skin on the face, rump, and genitalia; a sternal scent-marking gland; and a "fatted" rump. Mandrills are seasonal breeders, and in other seasonally-breeding primate species members of both sexes may show increased expression of secondary sexual characteristics during the mating season. We examined changes in male secondary sexual adornments and testosterone levels, in relation to seasonal changes in the female reproductive cycle and sexual skin morphology, in two semifree-ranging mandrill groups. Females showed circannual changes in sexual skin tumescence, and periods of tumescence peaked from May-July in a long-established group. However, formation of a second, smaller group, two years previous to commencement of the study, disrupted the seasonal pattern of sexual skin tumescence and births. As the groups occupied adjacent enclosures, it appears that social factors, as well as physical environment, affected the seasonal patterning of reproduction in females. Male mandrills, by contrast, did not exhibit marked circannual changes in secondary sexual traits. Although adult male testicular volume and circulating testosterone levels increased significantly during the mating season, sexual skin coloration and rump "fattedness" showed no consistent changes with season. There was some evidence to suggest that maturing males (ages 5-8 yr) showed increased development of red sexual skin during mating periods, but once males had fully developed secondary sexual adornments, they remained stable throughout the year. The possible reasons for this are discussed in relation to intermale competition and social organization in mandrills.     

Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx).

Previous studies of semifree-ranging mandrills identified two morphological and social variants of the adult male, based on behavioral and secondary sexual characteristics. "Fatted" males are social, with highly developed sex skin coloration, large testes, high plasma testosterone levels, and fat rumps; while "nonfatted" males are peripheral or solitary, with paler sex skin, smaller testes, lower plasma testosterone, and slimmer rumps. We present a detailed study of morphology and group association for 10 adult male mandrills, living in two semifree-ranging groups in Gabon, in order to relate differences between males to dominance rank. The results show that rather than existing as two distinct morphotypes, male mandrills represent a continuous spectrum of possibilities between social males with fully developed secondary sexual characteristics, and solitary males with muted secondary sexual characteristics. Alpha males (N = 2) had the highest testosterone levels, the most colorful sex skin, and the most active sternal glands, and were the only males to spend 100% of their time with the social group. Rank relationships between nonalpha males (N = 8) were not always clear, but all subordinate males had lower testosterone levels and less development of the secondary sexual adornments, and were less group-associated than alpha males. These findings suggest that only alpha males have sufficient testosterone to develop full secondary sexual characteristics, and we propose possible socioendocrine mechanisms underlying the suppression of testosterone and secondary sexual development in subordinate adults. We discuss differences in secondary sexual development in relation to reproductive strategies, and discuss the evolution of alternative reproductive morphs in primates.     

Sex-limited expression of ornamental feathers in birds

Extravagant secondary sexual characters show sexual size dimorphismin some species but are completely sex limited in others. Sexualornamentation has been hypothesized to benefit mainly malesthrough sexual selection, but the costs of secondary sexualcharacters initially would be experienced by both sexes. Theevolution of sexual size dimorphism of ornaments and, eventually, the complete sex-limited expression of these characters, willdepend on the effects of sexual and natural selection on thetwo sexes. A phylogenetic analysis controlling for similaritiesdue to common ancestry of 60 independent evolutionary originsof feather ornamentation in birds was used to investigate ecologicalfactors correlated with sexual size dimorphism and sex-limited expression of secondary sexual characters. When the size ofan ornament is large relative to body size, the trait willbe particularly costly for females, resulting in selectionfor increased sexual size dimorphism of the ornament. Indeed,sexual size dimorphism of ornaments was positively related to the relative size of male ornaments but was unrelated torelative size of female ornaments. Species with polygynousand lekking mating systems with little or no male parentalcare (in particular nest building and incubation) demonstratedsex-limited expression of ornaments as compared to monogamous species. Species with no food provisioning of offspring by themale showed a trend for increased sexual size dimorphism ofornaments. Therefore, large natural selection costs duringreproduction imposed by the expression of secondary sexualcharacters are related to the evolution of sexual size dimorphismof ornaments and eventually their complete loss from females.