Sex roles in the ghost moth Hepialus humuli (L.) and a review of mating in the Hepialidae (Lepidoptera)

Recently it has been found that female Lepidoptera belonging to diverse families actively court their males, rather than play a merely passive role. Male and female Hepialus humuli have been reported to come together in three different ways: (1) females are attracted to groups or ‘leks’ of white, hovering males by visual stimuli; (2) females are attracted to the males by olfactory-substances produced on the hind-tibial brushes of the males; (3) males are attracted to sedentary females by olfactory stimuli. During my study I observed H. humili males flying on a total of 21 nights in two different parts of England. The males hovered in groups for about 20 min each evening, starting and stopping their flights in synchrony. Timing depended on light intensity, northern moths flying later in the summer evenings than southern moths. I observed a total of 18 matings. Normally, a female from outside a male lek flew into the group and up to one of the males. This male then usually followed her to a settling position, where mating took place. In a few cases females touched males; in one case a female struck a male in the air so that both fell to the ground and were copulating when examined. Photographs of hovering males show that their hind tibial brushes are fully everted in flight. The organs are folded against the body when the moth is mating, at rest or dead. Whilst hovering, the males are apparently emitting pheromones which function as primary attractants, rather than as the aphrodisiacs of many other lepidopteran males. The mating behaviour of hepialids is reviewed. It is concluded that all studied hepialids which have male brush organs (some Hepialus and Oncopera, Sthenopis, Zenophassus) exhibit similar flight and mating behaviour: males hover, sit or loop back and forth on the spot in leks; females fly into male aggregations and mate there (although some published observations suggest otherwise). In contrast, hepialids such as Fraus, Oxycanus and other Hepialus that lack male brush organs have mating behaviour in which the males are the active partner, a more standard lepidopteran method. In view of the controversies surrounding mating in hepialids, future systematic and behavioural work on Hepialidae throughout the world will be worthwhile.     

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load‐lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female‐specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load‐lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild‐caught male R. longicauda collected during copulation were experiencing load‐lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load‐lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.     

The flexible lek: Phymatopus hecta the gold swift demonstrates the evolution of leking and male swarming via a hotspot (Lepidoptera: Hepialidae)

Leking moths present an evolutionary problem in their apparently simultaneous reversal of male–female attraction. The mating system of Phymatopus (or Hepialus) hecta embraces an unusually wide range of procedures. Both males and females use medium‐range olfactory attractants (also probably visual signals), and both sexes will lure, and both will approach, the other, either when flying or perched. This produces an ‘infinite variety’ which includes the classic moth mating procedure (males fly to sessile female); a typical lek procedure (female flies to sessile male); a mating swarm (hovering male follows passing female); and intermediates such as a mutual courtship dance. Male behaviour includes a flying display, two sessile displays, and an escalating war of attrition. The system is versatile, persistent, and probably evolutionarily stable. The lek site has a high density of perches suitable for copulation which facilitate predator‐escape by means of a dead drop. The whole supports a model for the evolution of resource‐based leks which commence with a concentration of females on a hotspot, leading to a concentration of males; and then an escalating process of sexual selection as males become increasingly attractive over a distance to females, and females use the males as a way of locating the resource. The main stabilizing pressure may be selection for efficient mate acquisition, and as with grouse leking systems, the precondition for evolution was probably having travelling females that actively sought a reproductive resource or a predator free space. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 184–201.     

Lesion studies of neural mechanisms underlying the mating dance of the silkmoth,Bombyx mori

Lesion studies were carried out to reveal neural mechanisms controlling a characteristic mating behavior, referred to as ‘mating dance’ in a maleBombyx mori which appears in reaction to the sex pheromone of the conspecific female. The experiments revealed 2 essential neural mechanisms involved in the mating dance. One is a flight motor system in the thorax, which organizes the wing vibration representing the mating dance. The other, a dance command element, is in the head ganglia. Once activated by the female sex pheromone, the latter can maintain its excitation for several minutes without additional stimulation. This long-lasting neuronal excitation was suggested to descend via cervical connectives to the thoracic ganglia and activate the flight motor system into operation.     

Genetic variability associated with hovering time inTabanus nigrovittatus Macquart (Diptera: Tabanidae)

The salt marsh horse fly, Tabanus nigrovittatusMacquart, exhibits two nonoverlapping daily periods of hovering and mating activity, which are correlated with different environmental temperatures. Allelic and genotypic frequencies of hovering males collected during the two periods were compared by electrophoresis of three polymorphic enzyme loci. Approximately 26% of early-hovering males possessed a Pgmallozyme that was absent in our sample of late-hovering males. However, based on other allozyme loci, we found no evidence for reproductive isolation between early and late hoverers. All the genetic data are consistent with the hypothesis that the Pgmpolymorphism is associated with behaviorally and physiologically distinct groups of males that, by all other criteria, form a single Mendelian population.     

Efficient inference of paternity and sibship inference given known maternity via hierarchical clustering

Pedigree and sibship reconstruction are important methods in quantifying relationships and fitness of individuals in natural populations. Current methods employ a Markov chain‐based algorithm to explore plausible possible pedigrees iteratively. This provides accurate results, but is time‐consuming. Here, we develop a method to infer sibship and paternity relationships from half‐sibling arrays of known maternity using hierarchical clustering. Given 50 or more unlinked SNP markers and empirically derived error rates, the method performs as well as the widely used package Colony, but is faster by two orders of magnitude. Using simulations, we show that the method performs well across contrasting mating scenarios, even when samples are large. We then apply the method to open‐pollinated arrays of the snapdragon Antirrhinum majus and find evidence for a high degree of multiple mating. Although we focus on diploid SNP data, the method does not depend on marker type and as such has broad applications in nonmodel systems.     

Precedence of the first male sperm in successive matings in the HymenopteraDiadromus pulchellus

In most insect species where double matings occur, sperm from the second male preferentially fertilize subsequent eggs. However, we demonstrate here that, as already shown for some other hymenopteran species, this is not the case in the ichneumonid waspDiadromus pulchellus (Wesmeal): sperm from the first male usually father all the female progeny. This precedence of the first male sperm is also observed in double matings involving an haploid male and a diploid sterile male, whichever is the first mating male. We discuss the consequences of this phenomenon from an evolutionary point of view.     

The evolution of the mating system of the Carpenter bee Xylocopa varipuncta(Hymenoptera: Anthophoridae)

The Carpenter bee, Xylocopa varipuncta , appears to have evolved a dispersed lek mating system. Males leave the natal nest in the late afternoon in March and April to hover for periods of up to two hours in the crowns of non-flowering trees growing in desert washes. Females and other males occasionally visit a hovering male, probably drawn by a sex pheromone. Resident males repel intruders of the same sex and attempt to induce females to alight on foliage, where mating occurs. The hovering territories do not contain nests, or potential nest sites, or food resources for females. Lek territoriality may have evolved in this species because nests are difficult to locate and the food-plants are evenly dispersed over a large area, making economical defence of patches of this resource unfeasible. Males are left with the option of demonstrating social dominance to potential mates through control of a superior landmark territory.     

Intra-Colonial Variability in the Dance Communication in Honeybees (Apis mellifera)

Honeybees have evolved numerous mechanisms for increasing colony-level foraging efficiency, mainly the combined system of scout-recruit division of labour and recruitment communication. A successful forager performs waggle dances on the surface of the comb where it interacts with nectar receivers and dance followers. A forager uses tremble dance when it experiences difficulty finding a receiver bee to unload food upon return to the hive. A bee colony containing numerous subfamilies may increase its efficiency in dance communication if dances are realized by particular groups of specialized individuals or subfamilies rather than by undifferentiated workers. In this study, we determined the subfamily frequencies of waggle and tremble dancers in a colony headed by a naturally mated queen, where the 17 subfamilies can be identified by microsatellite genetic markers. Our results demonstrate that a genetic component is associated with the dance communication in honeybees. More than half of the waggle dances and the tremble dances were performed by workers from only four subfamilies in each case.     

Sexual conflicts, loss of flight, and fitness gains in locomotion of polymorphic water striders

In insect wing polymorphism, morphs with fully developed, intermediate, and without wings are recognized. The morphs are interpreted as a trade‐off between flight and flightlessness; the benefits of flight are counterbalanced by the costs of development and the maintenance of wings and flight muscles. Such a trade‐off has been widely shown for reproductive and developmental parameters, and wing reduction is associated with species of stable habitats. However, in this context, the role of water locomotion performance has not been well explored. We chose seven water striders (Heteroptera: Gerridae) as a model to study this trade‐off and its relation to sexual conflicts, namely, Aquarius elongatus (Uhler), Aquarius paludum (Fabr.), Gerris insularis (Motschulsky), Gerris nepalensis Distant, Gerris latiabdominis Miyamoto, Metrocoris histrio (White), and Rhagadotarsus kraepelini Breddin. We estimated the locomotion performance as the legs’ stroke force, measured on tethered specimens placed on water with a force transducer attached to their backs. By dividing force by body weight, we made performance comparisons. We found a positive relationship between weight and force, and a negative one between weight and the force‐to‐weight ratio among species. The trade‐off between water and flight locomotion was manifested as differences in performance in terms of the force/weight ratio. However, the bias toward winged or wing‐reduced morphs was species dependent, and presumably related to habitat preference. Water strider species favouring a permanent habitat (G. nepalensis) showed higher performance in the apterous morph, but in those favouring temporary habitats (A. paludum and R. kraepelini) morphs’ performance did not differ significantly. Males had higher performance than females in all but three species studied (namely, A. elongatus, G. nepalensis, and R. kraepelini); these three have a type II mating strategy with minimized mating struggle. We hypothesized that in type I mating system, in which males must struggle strongly to subdue the female, males should outperform females to copulate successfully. This was not necessarily true among males of species with type II mating.     

Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity

Sex-ratio distorters are found in numerous species and can reach high frequencies within populations. Here, we address the compelling, but poorly tested, hypothesis that the sex ratio bias caused by such elements profoundly alters their host's mating system. We compare aspects of female and male reproductive biology between island populations of the butterfly Hypolimnas bolina that show varying degrees of female bias, because of a male-killing Wolbachia infection. Contrary to expectation, female bias leads to an increase in female mating frequency, up to a point where male mating capacity becomes limiting. We show that increased female mating frequency can be explained as a facultative response to the depleted male mating resources in female biased populations. In other words, this system is one where male-killing bacteria trigger a vicious circle of increasing male fatigue and female promiscuity.     

Danger of zooplankton feeding: the fluid signal generated by ambush-feeding copepods

Zooplankton feed in any of three ways: they generate a feeding current while hovering, cruise through the water or are ambush feeders. Each mode generates different hydrodynamic disturbances and hence exposes the grazers differently to mechanosensory predators. Ambush feeders sink slowly and therefore perform occasional upward repositioning jumps. We quantified the fluid disturbance generated by repositioning jumps in a millimetre-sized copepod (Re ∼ 40). The kick of the swimming legs generates a viscous vortex ring in the wake; another ring of similar intensity but opposite rotation is formed around the decelerating copepod. A simple analytical model, that of an impulsive point force, properly describes the observed flow field as a function of the momentum of the copepod, including the translation of the vortex and its spatial extension and temporal decay. We show that the time-averaged fluid signal and the consequent predation risk is much less for an ambush-feeding than a cruising or hovering copepod for small individuals, while the reverse is true for individuals larger than about 1 mm. This makes inefficient ambush feeding feasible in small copepods, and is consistent with the observation that ambush-feeding copepods in the ocean are all small, while larger species invariably use hovering or cruising feeding strategies.     

First report on the emergency dance of Apis cerana japonica,which induces odorous plant material collection in response to Vespa mandarinia japonica scouting

Previously, we observed several instances in which Apis cerana japonica performed dancing around the hive entrance and smeared plant materials there immediately after scouting of Vespa mandarinia japonica. In this study, we conducted a series of attack simulation experiments with three hornet species to investigate whether the hive entrance dance is a specific response to V. m. japonica scouting. We also tracked dancing bees and dance‐follower bees to observe whether they perform hive entrance smearing. Only V. m. japonica scouting induced dancing, and we confirmed that dancing and dance‐follower bees performed smearing behavior at the hive entrance. These results suggest that the hive entrance dance informs nestmates of a specific emergency and of the urgent need to collect odorous plant materials as a counter‐attack strategy.     

REINFORCEMENT IN CHORUS FROGS: LIFETIME FITNESS ESTIMATES INCLUDING INTRINSIC NATURAL SELECTION AND SEXUAL SELECTION AGAINST HYBRIDS

Maladaptive hybridization is hypothesized to be an important force driving the evolution of reproductive isolation between closely related species. Because the magnitude and direction of selection can vary across a life cycle, an accurate understanding of the ubiquity of reinforcement requires fitness to be estimated across the life cycle, but the literature is surprisingly depauperate of such studies. We present fitness estimates of laboratory‐raised hybrids between the chorus frogs Pseudacris feriarum and Pseudacris nigrita—two species that have undergone reproductive character displacement where they come into secondary contact. By studying viability, mating success, and fertility across the life cycle, we find strong support for reinforcement as the force driving displacement in this system. Specifically, we find hybrid fitness is reduced by 44%. This reduction results from both sexual selection against hybrid males and natural selection on male fertility, but not viability selection. Sexual selection against hybrid males is four times stronger than natural selection. Hybrid female fitness is not reduced, however, suggesting that Haldane's rule may be operating in this system if males are heterogametic. We also found higher variation in hybrid male fertilization success relative to P. feriarum males, suggesting that the hybrid incompatibility genes are polymorphic within one or both of the parent species.     

Eusocial bee male aggregations: spatially and temporally separated but genetically homogenous

Male insects mostly aggregate near sites where sexually reproductive virgin females are found and where mating occur. This reproductive strategy is quite common in Hymenoptera and appears to decrease the chances of inbreeding. In Hymenoptera, inbred mating frequently result in sterile diploid males. Production of diploid males may reach high proportions in small bee populations, and it usually lead to population extinction within a small number of generations. Aggregation of males during a short period of time allow the mixing of local genes. In this paper, we analyzed male aggregations of Tetragonisca angustula (Latreille) (Hymenoptera: Apidae), a eusocial stingless bee, using microsatellite molecular markers. We used population genetic statistics for haplodiploid organisms to address genetic structuring among male aggregations. Our findings indicate that, in general, male aggregations of T. angustula occurring over short time scales and in close proximity are genetically homogeneous as if a single aggregation. We conclude that T. angustula males randomly disperse within a population looking for mating chances rather than settle on a distinct male aggregation. This behavior seems to contribute to the reduction of inbreeding in this species.     

Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

We investigate the plausibility of sympatric speciation through a modelling study. We built up a series of models with increasing complexity while focussing on questioning the realism of model assumptions by checking them critically against a particular biological system, namely the sympatric benthic and limnetic species of threespine stickleback in British Columbia, Canada. These are morphologically adapted to their feeding habits: each performs better in its respective habitat than do hybrids with intermediate morphology. Ecological character displacement through disruptive selection and competition, and reinforcement through mating preferences may have caused their divergence. Our model assumptions include continuous morphological trait(s) instead of a dimorphic trait, and mating preferences based on the same trait(s) as selected for in food competition. Initially, morphology is intermediate. We apply disruptive selection against intermediates, frequency-dependent resource competition, and one of two alternative mating preference mechanisms. Firstly, preference is based on similarity where mating preference may result from “imprinting” on conspecifics encountered in their preferred foraging habitat. Here, speciation occurs easily—ecological hybrid inferiority is not necessary. Hybrid inferiority reinforces the stringency of assortative mating. Secondly, individual preferences exist for different trait values. Here, speciation occurs when linkage disequilibrium between trait and preference develops, and some hybrid inferiority is required. Finally, if the morphology subject to disruptive selection, frequency-dependent competition, and mate choice, is coded for by two loci, linkage disequilibrium between the two loci is required for speciation. Speciation and reinforcement of stringency of choosiness are possible in this case too, but rarely. Results demonstrate the contingency of speciation, with the same starting point not necessarily producing the same outcome. The study resulted in flagging issues where models often lack in biological realism and issues where more empirical studies could inform on whether assumptions are likely valid.     

Kin‐bias,breeding site selection and female fitness in a cannibalistic Neotropical frog

Resource availability influences sexual selection within populations and determines whether behaviours such as territoriality or resource sharing are adaptive. In Thoropa taophora, a frog endemic to the Atlantic Coastal Rainforest of Brazil, males compete for and defend limited breeding sites while females often share breeding sites with other females; however, sharing breeding sites may involve costs due to cannibalism by conspecific tadpoles. We studied a breeding population of T. taophora to determine (i) whether this species exhibits polygynous mating involving female choice for territorial males and limited breeding resources; (ii) whether limited breeding resources create the potential for male–male cooperation in defence of neighbouring territories; and (iii) whether females sharing breeding sites exhibit kin‐biased breeding site choice, possibly driven by fitness losses due to cannibalism among offspring of females sharing sites. We used microsatellites to reconstruct parentage and quantify relatedness at eight breeding sites in our focal population, where these sites are scarce, and in a second population, where sites are abundant. We found that at localities where the appropriate sites for reproduction are spatially limited, the mating system for this species is polygynous, with typically two females sharing a breeding site with a male. We also found that females exhibit negative kin‐bias in their choice of breeding sites, potentially to maximize their inclusive fitness by avoiding tadpole cannibalism of highly related kin. Our results indicate that male territorial defence and female site sharing are likely important components of this mating system, and we propose that kinship‐dependent avoidance in mating strategies may be more general than previously realized.     

Hovering sunbirds in the Old World: occasional behaviour or evolutionary trend?

The nectarivory of sunbirds in the Old World and hummingbirds in the New World evolved independently. While both groups are specialised in their feeding apparatuses, hummingbirds are moreover famous for their adaptations to sustained hovering flight. Recently, an example of a pollination system of the invasive plant Nicotiana glauca has been used to show that less adapted sunbirds also are frequently able to hover. Nevertheless, the question has remained why plants adapted to bird hovering pollination do not occur outside the New World. In this paper we show that the long‐peduncle Cameroonian Impatiens sakeriana is not capable of autonomous selfing and can be pollinated only by two often hovering sunbirds, the Cameroon sunbird Cyanomitra oritis and the northern double‐collared sunbird Cinnyris reichenowi. Our study revealed that this plant is highly specialised for pollination by C. oritis. Cinnyris reichenowi hovers less frequently and often thieves nectar by piercing the flower spur when perching. This study shows that pollination systems occurring in the Old World follow similar evolutionary trends as systems including hovering hummingbirds in the New World.     

Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World

The bird pollination systems of the New and Old Worlds evolved independently, and differ in many aspects. New World plants are often presented as those adapted to hovering birds while Old World plants to perching birds. Most Neotropical studies also demonstrate that in hummingbird species rich assemblages, only a small number of highly specialized birds exploits the most specialized plants with long corollas. Nevertheless, recent research on bird–plant pollination interactions suggest that sunbird pollination systems in the Old World have converged more with the highly specialized hummingbird pollination systems than previously thought. In this study we focus on the pollination systems of the bird pollination syndrome Impatiens species on Mt. Cameroon, West Africa. We show that despite the high diversity of sunbirds on Mt. Cameroon, only Cyanomitra oritis appear to be important pollinator of all Impatiens species. This asymmetry indicates the absence of pair wise co‐evolution and points to a diffuse co‐evolutionary process resulting in guilds of highly specialized plants and birds; a situation well known from hummingbirds and specialized plant communities of the New World. Additionally, the herbaceous habits of Impatiens species, the frequent adaptations to pollination by hovering birds, and the habitat preference for understory in tropical forests or epiphytic growth, resemble the highly specialized Neotropical plants. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 127–133.     

Selective advantage for sexual reproduction with random haploid fusion

This article develops a simplified set of models describing asexual and sexual replication in unicellular diploid organisms. The models assume organisms whose genomes consist of two chromosomes, where each chromosome is assumed to be functional if it is equal to some master sequence σ₀, and non-functional otherwise. We review the previously studied case of selective mating, where it is assumed that only haploids with functional chromosomes can fuse, and also consider the case of random haploid fusion. When the cost for sex is small, as measured by the ratio of the characteristic haploid fusion time to the characteristic growth time, we find that sexual replication with random haploid fusion leads to a greater mean fitness for the population than a purely asexual strategy. However, independently of the cost for sex, we find that sexual replication with a selective mating strategy leads to a higher mean fitness than the random mating strategy. The results of this article are consistent with previous studies suggesting that sex is favored at intermediate mutation rates, for slowly replicating organisms, and at high population densities. Furthermore, the results of this article provide a basis for understanding sex as a stress response in unicellular organisms such as Saccharomyces cerevisiae (Baker’s yeast).