Physical Restraint or Stimulation? The Function(s) of the Modified Front Legs of Male Archisepsis diversiformis (Diptera, Sepsidae)

Four hypotheses that could explain the elaborate species-specific morphology of the clasping organs on the front legs of male Archisepsis diversiformis flies were tested: direct male–male combat, mechanical fit, male–female conflict of interests, and male stimulation of the female. Experimental modification of the shape of the male clasper and of the female wing base where the male clasped the female both strongly reduced the chances that a mount would result in copulation. This reduction was not predicted by the male–male combat hypothesis but was predicted by the others. Males in the field did nave to fight other males to remain mounted on females, as expected by the male–male combat hypothesis. Reduced male copulatory success was not due to inferior male ability to grasp and hold onto the female's wings, as predicted by the mechanical fit and male–female conflict hypotheses but to a reduction in the likelihood that the female would allow intromission, as predicted by the stimulation hypothesis. By a process of elimination, and in combination with data from a previous morphological study, the data support the hypothesis that the species-specific aspects of grasping organs in these flies function to stimulate females. Further behavioral data will be needed to test alternative possibilities.     

Lack of morphological coevolution between male forelegs and female wings in Themira (Sepsidae: Diptera: Insecta)

The complex, species-specific foreleg armature in males of the genus Themira (Diptera: Sepsidae) provides an ideal system for testing competing hypotheses for the evolution of sexually dimorphic character divergence. In sepsid flies, the male holds onto the female by clasping her wing base with his modified forelegs. In the present study, we document the male leg and the female wing morphology using scanning electron microscopy and confocal microscopy. We use a phylogenetic tree for Themira to reconstruct male foreleg and female wing evolution and demonstrate that the male legs have evolved elaborate structures with little or no corresponding changes in wing morphology. This lack of interspecific variation in female wings is not in agreement with the hypothesis of a morphological 'evolutionary arms race' between males and females. However, there is also no evidence for sex-specific wing differences in sensory organs on the wing base that may explain how females could assess males according to Eberhard's 'cryptic female choice' hypothesis. Finally, our study reveals the function of several novel morphological clasping structures and documents that the male foreleg characters in Themira are highly homoplastic. Male forelegs in two clades evolve considerably faster than in other species or clades. These two clades include Themira superba and Themira leachi , species that have some of the most dramatically modified forelegs known in Diptera.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 227–238.     

Copulation behaviour of Glossina pallidipes (Diptera: Muscidae) outside and inside the female, with a discussion of genitalic evolution

If species-specific male genitalia are courtship devices under sexual selection by cryptic female choice, then species-specific aspects of the morphology and behaviour of male genitalia should often function to stimulate the female during copulation. The morphology and behaviour of the complex, species-specific male genitalia of the tsetse fly, Glossina pallidipes Austen, were determined from both direct observations and dissections of flash-frozen copulating pairs; we found that some male genitalic traits probably function to stimulate the female, while others function to restrain her. The male clamps the ventral surface of the female's abdomen tightly with his powerful cerci. Clamping does not always result in intromission. Clamping bends the female's body wall and her internal reproductive tract sharply, posteriorly and dorsally, and pinches them tightly. The male performed sustained, complex, stereotyped, rhythmic squeezing movements with his cerci that were not necessary to mechanically restrain the female and appeared instead to have a stimulatory function. Six different groups of modified setae on and near the male's genitalia rub directly against particular sites on the female during squeezing. The designs of these setae correlate with the force with which they press on the female and the probable sensitivity of the female surfaces that they contact. As expected under the hypothesis that these structures are under sexual selection by female choice, several traits suspected to have stimulatory functions have diverged in G. pallidipes and its close relative, G. longipalpis. Additional male non-genitalic behaviour during copulation, redescribed more precisely than in previous publications, is also likely to have a courtship function. The elaborate copulatory courtship behaviour and male genitalia may provide the stimuli that previous studies showed to induce female ovulation and resistance to remating.     

Sexually antagonistic coevolution in insects is associated with only limited morphological diversity

Morphological traits involved in male-female sexual interactions, such as male genitalia, often show rapid divergent evolution. This widespread evolutionary pattern could result from sustained sexually antagonistic coevolution, or from other types of selection such as female choice or selection for species isolation. I reviewed the extensive but under-utilized taxonomic literature on a selected subset of insects, in which male-female conflict has apparently resulted in antagonistic coevolution in males and females. I checked the sexual morphology of groups comprising 500-1000 species in six orders for three evolutionary trends predicted by the sexually antagonistic coevolution hypothesis: males with species-specific differences and elaborate morphology in structures that grasp or perforate females in sexual contexts; corresponding female structures with apparently coevolved species-specific morphology; and potentially defensive designs of female morphology. The expectation was that the predictions were especially likely to be fulfilled in these groups. A largely qualitative overview revealed several surprising patterns: sexually antagonistic coevolution is associated with frequent, relatively weak species-specific differences in males, but male designs are usually relatively simple and conservative (in contrast to the diverse and elaborate designs common in male structures specialized to contact and hold females in other species, and also in weapons such as horns and pincers used in intra-specific battles); coevolutionary divergence of females is not common; and defensive female divergence is very uncommon. No cases were found of female defensive devices that can be facultatively deployed. Coevolutionary morphological races may have occurred between males and females of some bugs with traumatic insemination, but apparently as a result of female attempts to control fertilization, rather than to reduce the physical damage and infections resulting from insertion of the male's hypodermic genitalia. In sum, the sexually antagonistic coevolution that probably occurs in these groups has generally not resulted in rapid, sustained evolutionary divergence in male and female external sexual morphology. Several limitations of this study, and directions for further analyses are discussed.     

Courtship and mating by the sandfly Phlebotomus duboscqi, a vector of zoonotic cutaneous leishmaniasis in the Afrotropical region

Courtship behaviour of males of the Afrotropical sandfly Phlebotomus duboscqi Neveu-Lemaire (Diptera: Psychodidae) involved mounting the female and clasping her 'waist' with the male coxites placed between the female's thorax and abdomen. This behaviour, which we call 'piggy-backing', was preceded by male wing beating, perhaps involving mate recognition and contact pheromones. It did not seem to be pre- or postcopulatory mate guarding. Piggy-backing was attempted by P. duboscqi males on females of other species (P. papatasi and P. perniciosus) and even on other male P. duboscqi. The majority of female P. duboscqi piggy-backed by males were already inseminated, and most of the courting did not lead to copulation. This, coupled with the presence of a mating plug (semen) in each spermatheca of inseminated females, suggests that female P. duboscqi are monogamous for at least the first gonotrophic cycle. Male courtship with piggy-backing was more intense when females could feed on a hamster than when a hamster was present but the females were denied access to the host. It is suggested that, when a hamster was available to the females, the conditions in the laboratory are similar to those in rodent holes, the natural habitat of P. duboscqi.     

Trauma, disease and collateral damage: conflict in cimicids

The bed bugs and bat bugs (Hemiptera: Cimicidae) are unusual in being a gonochorist (separate male and female genders) taxon with obligate traumatic insemination. Males of all the species in this family have a lanceolate paramere (intromittent organ) which they use to pierce the female's body wall and inseminate directly into her haemocoel, despite the presence of a functional female genital tract. Mating is tightly linked to the feeding cycle in Cimex lectularius, the common bed bug. In this paper, I examine key aspects of the reproductive anatomy and behaviour of C. lectularius that underpin the nature of the conflict over mating rate in this species. I then examine the consequences of traumatic insemination for female fitness and examine potential mechanisms that might underpin those costs. Finally, the collateral consequences of the male reproductive tactic on other males of C. lectularius and the African bat bug, Afrocimex constrictus are examined.     

Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice

Male structures specialized to contact females during sexual interactions often diverge relatively rapidly over evolutionary time. Previous explanations for this pattern invoked sexual selection by female choice, but new ideas emphasize possible sexually antagonistic coevolution resulting from male-female conflict over control of fertilization. The two types of selection have often not been carefully distinguished. They do not theoretically exclude one another, but they have not necessarily had equally important roles in producing rapid evolutionary divergence. To date, most recent empirical studies of antagonistic coevolution have emphasized only a few taxa. This study uses the abundant but little-used data in the taxonomic literature on morphology to evaluate the roles of antagonistic coevolution and traditional female choice over a wide taxonomic spectrum (61 families of arthropods, mostly insects and spiders). Groups with species-specific male structures that contact females were checked for coevolution of species-specific female structures that are contacted by the male and that have mechanical properties that could potentially defend her against the male. Facultatively deployable, species-specific female defensive structures, a design that would seem likely to evolve frequently under the sexually antagonistic coevolution hypothesis, were completely absent (0% of 106 structures in 84 taxonomic groups). Although likely cases of sexually antagonistic coevolution exist, using conservative criteria, 79.2% of the 106 structures lacked even potentially defensive female coevolution. A common pattern (53.8% of 106) was a nearly complete absence of female change in areas contacted by species-specific male structures. Post-hoc arguments invoking possible coevolution of defensive female behavior instead of morphology, or of female sensitivities and responses to male sensory traps, could enable the sexually antagonistic coevolution hypothesis to explain these data. No case of such coevolution of female behavior or sensitivities has been demonstrated, and there are additional reasons to doubt that they are general explanations for the data presented here. Detailed studies of female resistance behavior could help illuminate several issues. The possibility of a greater role for antagonistic coevolution in reproductive physiology than in morphology and the possibility that female choice and sexually antagonistic coevolution have both been important in some lineages are discussed.     

A phylogenetic analysis of the evolution of sexual dimorphism and mating systems in water striders (Hemiptera: Gerridae)

Conflicts over mating decisions characterize the sexual behaviour of many insects, in particular when males encounter females that already carry enough sperm to fertilize their eggs, since a mating often will inflict greater costs than benefits upon females. Therefore, coevolutionary models predict adaptation and counter-adaptation by the sexes in a battle to control the outcome of sexual encounters. A phylogenetic analysis was performed on patterns of sexual dimorphism and mating systems within water striders (Hemiptera, Gerridae). Phylogenetic effects or 'constraints' have significantly shaped patterns of sexual dimorphism in female/ male size ratios, legs and genitalia of males, and the structure of the female abdomen. Males of ancestral gerrids were probably slightly smaller than conspecific females, had powerful fore legs adapted to grasp the female's thorax during mating, and had clasping genitalic structures suited to grasp or pinch the female posteriorly. Most gerrids have a female/male size ratio between 1.05 and 1.14, but more pronounced sexual size ratios (above 1.25) have independently evolved several times in the family, usually in association with extended post-copulatory mate guarding. The comparative, phylogenetic analysis suggests coevolution of female anticlasper and male clasping devices for the clade comprising the subfamilies Cylindrostethinae, Ptilomerinae, and Halobatinae while female anticlasper devices have evolved in the absence of male clasping genitalia in the Gerrinae. The ancestral and most common mating system in gerrids is 'scramble competition polygyny' from which has evolved 'resource defence polygyny' at least four times independently of each other. The phylogenetic effects on patterns of mating behaviour are much less obvious, as exemplified by the large amount of interspecific variation in some genera.     

INTRASEXUAL COMPETITION ALONE FAVORS A SEXUALLY DIMORPHIC ORNAMENT IN THE RUBYSPOT DAMSELFLY HETAERINA AMERICANA

I studied the sex-limited red spots on the wings of male rubyspot damselflies (Hetaerina americana) in relation to territoriality and fitness in the wild. Both observational and experimental (wing spot manipulation) studies indicated that wing spots were selected through competition among males for mating territories, not through female choice or direct competition for females. Males with naturally or artificially large wing spots were more successful at holding territories and consequently mated at higher rates than males with relatively small wing spots. In contrast, sexual selection on male body size appeared to operate among nonterritorial males at the clasping stage of the mating sequence, perhaps because larger males were better at clasping females forcibly. Of four models proposed to explain the evolution of ornaments through territory competition, only the agonistic handicap model makes predictions consistent with the results of this study.     

Copulatory behaviour of the potato tuber moth, Phthorimaea operculella

ABSTRACT. Copulatory behaviour of the potato tuber moth, Phthorimaea operculella , was observed in a small glasshouse. The behavioural chain is started by the female 'calling'. Males responded to the female's sex pheromone by searching in her vicinity. When the males 'recognized' the female, they attempted copulation. This behaviour was released, however, by a wide variety of models, including dried whole male and female bodies, similarly sized rolls of paper with male or female wings attached, rolls of paper covered in wing scales, and even flat surfaces covered in wing scales (provided the surface was much larger than a moth). It is concluded that the mechanical stimulus from the scales is an important stimulus for evoking copulation.     

Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

In contrast to male genitalia that typically exhibit patterns of rapid and divergent evolution among internally fertilizing animals, female genitalia have been less well studied and are generally thought to evolve slowly among closely-related species. As a result, few cases of male-female genital coevolution have been documented. In Drosophila, female copulatory structures have been claimed to be mostly invariant compared to male structures. Here, we re-examined male and female genitalia in the nine species of the D. melanogaster subgroup. We describe several new species-specific female genital structures that appear to coevolve with male genital structures, and provide evidence that the coevolving structures contact each other during copulation. Several female structures might be defensive shields against apparently harmful male structures, such as cercal teeth, phallic hooks and spines. Evidence for male-female morphological coevolution in Drosophila has previously been shown at the post-copulatory level (e.g., sperm length and sperm storage organ size), and our results provide support for male-female coevolution at the copulatory level.     

Behavioural correlates with hemipenis morphology in New World natricine snakes

Copulatory organs (hemipenes) of male snakes vary markedly among species in shape and ornamentation. We suggest that sexual conflict over copulation duration may have shaped the evolution of hemipenis morphology, favouring more elaborate organs in species in which a long duration of copulation is especially beneficial to males, despite the associated costs to females. To test this proposition, we compare mating behaviour between two species of gartersnakes differing in hemipenis morphology. In addition, we review data on copulation duration and hemipenis morphology and relate hemipenis morphology to phylogeny among of New World natricines. As predicted, copulation duration was significantly shorter in the common gartersnake ( Thamnophis sirtalis ), a species with simple subcylindrical hemipenes, than in the plains gartersnake ( Thamnophis radix ), a species with more complex, bilobed organs. Furthermore, female T. radix frequently exhibited vigorous body rolls during copulation, a behaviour associated with copulation termination, whereas female T. sirtalis never exhibited this behaviour. Copulations were of shorter duration when female T. radix (but not T. sirtalis ) more greatly exceeded males in body size, suggesting that females can more easily disengage from small males. Our review of New World natricines provides only weak evidence for an association between copulation duration and hemipenis morphology. Our mapping of hemipenis morphology onto the New World natricine phylogeny suggests that hemipenis morphology is evolutionarily plastic; both simple and bilobed hemipenes occur in all three major natricine clades, as well as in two of three gartersnake subclades and several sister-species pairs.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 110–120.     

Secondarily reduced foreleg armature in Perochaeta dikowi sp.n. (Diptera: Cyclorrhapha: Sepsidae) due to a novel mounting technique

Abstract.  The males of almost all sepsid species have strongly modified forelegs that are used to clamp the female's wingbase during mounting. Here, we describe a new species in the genus Perochaeta whose males have unmodified forelegs. We use DNA sequence data for ten genes to reconstruct the position of Perochaeta on the phylogenetic tree for Sepsidae, and reveal that the lack of foreleg armature in Perochaeta dikowi sp.n. is secondary. Through the study of the mating behaviour of the new species, we demonstrate that the loss of armature is correlated with a new mounting technique during which the males of P. dikowi do not use the foreleg to clamp the female's wingbase. Instead, the male approaches the female from behind and bends his abdomen forwards in order to establish genital contact. Our study shows how data from morphology, phylogenetics, and behavioural biology can complement each other to yield a deeper understanding of how changes in morphology and behaviour are correlated.     

Path analysis and the relative importance of male-female conflict, female choice and male-male competition in water striders

Three major behavioural mechanisms underlying sexual selection in many systems are male-male competition, female choice and male-female conflict. We used path analysis to evaluate the relative importance of these mechanisms in generating sexual selection on a suite of male traits in the stream-dwelling water strider, Aquarius remigis. To gather data for the analysis, we quantified the morphology (total length, limb length, forefemur width, genital length), behaviour (activity), mating frequency, mean mating duration and overall mating success of 96 adult males over a 10-day period. Males varied considerably in mating success. Over the 10 days, individual males mated 0-14 times, spending 0-67% of their time in copula. Path analysis showed that male-male competition was important in favouring larger males with longer limbs that tended to be more active. Active males should encounter females more frequently. In water striders, almost all male-female encounters result in intense premating struggles pitting female resistance to mating against male insistence. This male-female conflict favoured larger males with longer genitalia. These traits help males overcome female resistance. Female choice was expressed via female-controlled variation in mate-guarding durations. Female choice favoured smaller males perhaps because they are lighter, less expensive ‘shields’ against harassment by other males. Male size thus affected mating success via all three behavioural mechanisms. Weak, overall sexual selection favouring larger males was the product of conflicting effects: male-female conflict strongly favouring larger males and male-male competition weakly favouring larger males, offset by female choice favouring smaller males. Separate analyses for warmer versus colder days showed that on colder days (daily high below 20 °C), male-male competition was the main mechanism generating variation in mating frequency, while on warmer days, both male-male competition and male-female conflict were important. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Female choice of sexually antagonistic male adaptations: a critical review of some current research

We contrast some recent uses of the concept of male-female conflict, with the type of conflict that is inherent in traditional Darwinian female choice. Females in apparent conflict situations with males may suffer reduced lifetime reproduction, but nevertheless benefit because they obtain sons with superior manipulative abilities. Female defences against male manipulations may not be 'imperfect' because of inability to keep pace with male evolution, but in order to screen males and favour those that are especially good manipulators. We examine the consequences of these ideas, and of the difficulties of obtaining biologically realistic measures of female costs, for some recent theoretical and empirical presentations of male-female conflict ideas, and find that male-female conflict in the new sense is less certain than has been commonly supposed. Disentangling previous sexual selection ideas and the new conflict of interest models will probably often be difficult, because the two types of payoffs are not mutually exclusive.     

Sperm transfer and mating in Ricinoides hanseni (Ricinulei: Arachnida)

Ricinuleid reproduction involves indirect sperm transfer using the highly modified distal podomeres of the third legs of the male. This is homologous with the apparatus and technique used by male spiders, which possess elaborate pedipalps. The interpretation of the method of sperm transfer is based upon morphological studies of the male's third legs and the female's genital atrium and the behaviour of males during mating. The male charges the emboli of his modified leg tarsi with sperm from his penis. After climbing on to the back of a receptive female he delicately and precisely places a modified tarsus in the genital atrium of the female. A series of lobes on the tip of part of the modified tarsus fit into a number of vesicular evaginations of the female's genital atrium. The lobes form part of the mechanism which provides a firm attachment of the male's tarsal elements with the female's genital atrium during sperm transfer. A tubular element of the modified tarsus fits into a spermatheca of the female. Sperm and seminal fluid are then injected from the male's embolus into the female's spermatheca.     

Sexual conflict in Gerris gillettei (Insecta: Hemiptera): intraspecific intersexual correlated morphology and experimental assessment of behaviour and fitness

The contemporary dynamics of sexually antagonistic coevolution caused by sexual conflicts have seldom been investigated at the intraspecific level. We characterized natural populations of Gerris gillettei and documented significant intersexual correlations for morphological traits previously related to sexual conflict in water striders. These results strongly indicate that sexually antagonistic coevolution contributed to population differentiation and resulted in different balances of armaments between the sexes within natural populations of this species. No-choice mating experiments further revealed that both male and male-female relative arms levels influence copulation duration. However, there were no asymmetries in reproductive behaviour and fitness between sympatric and allopatric mating pairs, suggesting that differentiation by sexual conflict was not sufficient to influence the outcome of mating interactions. Altogether, these results question the relative importance of female connexival spines vs. genitalia traits in mediating pre- and post-copulatory conflict in Gerris.     

Effect of non‐lethal sampling on life‐history traits of the protected moth Graellsia isabelae (Lepidoptera: Saturniidae)

Abstract 1. Non‐lethal genetic surveys in insects usually extract DNA from a leg or a piece of wing. Although preferable to lethal sampling, little is known about the effect of leg/wing non‐lethal sampling on fitness‐related traits. 2. Graellsia isabelae (Graells, 1849) is a European moth protected by the Habitats Directive and the Bern Convention. Conservation genetics surveys on this species should therefore use non‐lethal sampling. 3. The present study aimed to (1) quantify the effects of both leg and hind‐wing tail sampling on survivorship and reproductive behaviour of adult males and females, and (2) assess the quality and quantity of DNA obtained from those tissues. 4. Both hind‐wing tails and mid‐legs proved to be good sources of high quality nuclear and mitochondrial DNA. DNA concentration was significantly higher when extracted from a large (130 mm²) piece of the hind‐wing tails than from about half of the mid‐leg. Using mark–release–recapture experiments with adults, it was found that neither mid‐leg nor hind‐wing tail sampling significantly reduced male survivorship or total number of matings. However, although mid‐leg sampling did not significantly affect female survivorship, it had a negative effect on female mating success. 5. Wing‐tail clipping on males appeared to be the best non‐lethal sampling procedure for G. isabelae. It is a fast procedure, similar to natural wing impairment, and did not significantly affect survival or mating behaviour.     

Flash communication systems of Japanese fireflies

Japanese fireflies range from nocturnal luminescent species to diurnal non-luminescent species. Their communication systems are classified into 6 types based on the following criteria: 1) Female responds to male's flashes after a fixed delay; 2) Male is directly attracted by female's light signal, the male perches on a leaf near the female, then the male changes his flashes with twinkling, and copulation behavior is released. However, the female may not respond to the male; 3) Male seeks female calling signal during the male's flying and synchronous flashing, then the male approaches the female, emitting flashes with various patterns, displaying walking-luminescing, sedentary signaling, chasing, and copulating; 4) Male is attracted by continuous luminescent signals of the female, and male perches near the female, then the male distinguishes the female's light organs shape. Thereafter, the male copulation behavior is released by her sex pheromone; 5) Male and female flight occurs in the daytime; when the male approaches the female, copulation is released by the female's pheromone; weak luminescent signals may be fulfilling the function of supplementary communication signals; 6) Luminescent signals have nothing to do with communication between male and female, and copulation is released by a sex pheromone.     

Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism

The degree and direction of sexual dimorphism across different species is commonly attributed to differences in the selection pressures acting on males and females. The extent of these differences is especially apparent in species that practise sexual cannibalism, where the female attempts to capture and eat a courting male. Here, we investigate the relationship between sexual dimorphism in size and leg length, sexual cannibalism and courtship behaviour in three taxonomic groups of orb-weaving spiders, using morphological data from 249 species in 36 genera. Females are larger than males in all three taxonomic groups, and males have relatively longer legs than females in both the Araneinae and Tetragnathidae. Across genera within each taxonomic group, male body size is positively correlated with both female body size and male leg length, and female body size is positively correlated with female leg length. Sexual size dimorphism is negatively correlated with relative male leg length within the Araneinae, but not within either the Tetragnathidae or the Gasteracanthinae. There was no negative correlation between sexual size dimorphism and relative female leg length in any taxonomic group. We argue that the relationship between sexual size dimorphism and relative male leg length within the Araneinae may be the result of selection imposed by sexual cannibalism by females.