Swarming Behavior, Sexual Dimorphism, and Female Reproductive Status in the Sex Role-Reversed Dance Fly Species Rhamphomyia marginata

Dance flies are predaceous insects which often form male mating swarms. In many species males prior to swarming catch an insect prey, which is presented to the female at mating. In Rhamphomyia marginata, females in contrast to males gather to swarm, while males carrying a prey visit swarms for mating. Here I describe the swarming and courtship behavior in R. marginata and provide data on sexual dimorphism and swarming female reproductive status. Females swarm in small clearings in the forests. There was no specific swarm-maker. The swarming period lasted for 2–3 h and peaked around sunset. Identical swarm sites were used each evening and for several years. The mean number of females in swarms (swarm sites with at least one female) was 9.9 ± 9.1 (range, 1–40; n = 107) in 1993 and 7.1 ± 7.0 (range, 1–35; n = 68) in 1994. No obvious competition between females in swarms was observed. The operational sex ratio in swarms was extremely female biased (all swarms, 0.04). Less than one-third of male visits to swarms resulted in mating and males were found more often in larger swarms. Nuptial prey consisted of male midges. Females seem to mate more than once. Swarming females had undeveloped eggs, whereas mated females in swarms had further developed eggs than unmated females. Amount of sperm in the spermatheca was correlated with egg size. Amount of sperm and egg size did not correlate with wet weight, wing length, or wing load, except for egg size and weight. The wing coloration pattern and shape in R. marginata females are unique among dance flies, being greatly enlarged (1.6 times larger than that of males) and bicolored (gray part, 60% of wing area). When females, instead of males, possess extravagant secondary sexual characters, it is predicted from sexual selection theory that females should compete for males and that males should be selective in their choice of partner. A sex-role reversal will evolve when assess to males limit female reproductive success. The dance fly species R. marginata, like Empis borealis, another dance fly species studied earlier and discussed here, seems to fit these predictions.     

Male body size and mating success in swarms of the mayfly Epeorus longimanus

Epeorus longimanus is a widely distributed mayfly in the western United States that forms relatively large mating swarms. The operational sex ratio of swarms is highly male biased and males are potentially polygynous, suggesting that male-male competition over mates may be intense. We investigated whether body size influenced male mating success in E. longimanus , as evidence of sexual selection. Males collected as mating pairs had significantly greater body lengths compared with males collected randomly from the swarm on each of six sampling dates examined, and had significantly greater head widths than males from random collections on two dates. There was no indication that large males occupied preferred positions within the swarm, and we suspect that the large male advantage may be due to greater success in pursuing females. We found no evidence of size-assortative mating in E. longimanus indicating that males attempt to male with every female encountered, consistent with the brief copulatory period in mayflies and overall low parental investment of males.     

Swarming and mating behavior in Ephemera orientalis Mclachlan, 1875 (Ephemeroptera: Ephemeridae) with morphological analyses

Swarming and mating behaviors of a mayfly species, Ephemera orientalis Mclachlan, 1875 were observed in 2015, 2016, and 2018 at a river bank of the Asahi River, Japan. Males started to make swarms between late April and middle May in 2016 and 2018. The numbers of mated pairs in a swarm correlated with the numbers of flying males in a swarm in 2016 and 2018. Swarms were formed during a limited period at dusk most probably because that interval is free from natural enemies. Males competed with each other to copulate with females in swarms. We clarified the function of the forelegs of males, which are significantly longer than those of females. Males used their forelegs to hold up a female from below. Besides forelegs, males have longer tails than females. We will discuss why sexual differences are found in these traits. Our results represent the first observation of swarm mating behavior in E. orientalis.     

Wing length and asymmetry of male Tokunagayusurika akamusi chironomid midges using alternative mating tactics

Male Tokunagayusurika akamusi chironomids have alternative mating tactics.One is to search for females on vegetation (ground mating),and the other is to wait for females in an aerial swarm (swarmmating). Simultaneous sampling of ground-unpaired and ground-pairedmales and of swarm-unpaired and swarm-paired males were performed.The average wing length and right-left wing length difference(wing asymmetry) were compared between males from the four differentcategories. Swarm-unpaired males were larger than ground-unpaired ones,swarm-paired males were larger than swarm-unpaired ones, and ground-pairedmales were not larger than ground-unpaired ones. Thus, large malestended to aggregate in swarms, and larger swarming males matedmore successfully. On the other hand, small males probably enjoyedmating on the ground, especially when large males swarmed. Thewing asymmetry was not significantly different between unpairedand paired males both within and between tactics. There wasa flat or U-shaped relationship between wing length and asymmetry,underpinning the lack of a symmetrical advantage of swarmingto large males. The right-left difference was not normally distributedin four of six samples of unpaired males but, in contrast, wasnot normally distributed in only one of six samples of pairedmales. The non-normal distributions were leptokurtic and includedoutliers. Removal of the outliers improved normality, suggestingthat males with extremely asymmetric wings were not successfulin mating.     

Swarming and mating ofChironomus yoshimatsui (Diptera: Chironomidae): Seasonal change in the timing of swarming and mating

Males ofChironomus yoshimatsui Martin et Sublette swarm at dusk, and copulate with females entering the swarm. It is likely in this species that, by restricting the time and place, swarming has the function of increasing the probability of the encounter between a sexually active male and a receptive female in the air. It is necessary that the timing of females taking wing coincides with that of males swarming. Field observations on swarming and mating from March to November showed that swarms and copulations occurred under lighter conditions at lower temperatures and under darker conditions at higher ones. It was suggested that both sexes may have a similar mechanism, depending on the temperature conditions, regulating the timing of taking wing.     

Age-associated male mating success in three swarming caddis fly species (Trichoptera: Leptoceridae)

Abstract. 1. In the three caddis fly species, Athripsodes albifrons (L.), A. cinereus (Curtis) and Mystacides azurea (L.) (Leptoceridae; Trichoptera), males swarm above the water surface of lakes or rivers. Receptive females fly to swarms and are chased and/or courted by males. After one of the swarming males has grasped an approaching female, the pair flies in tandem to the shore where they copulate.
2. In males, wing wear indices were negatively correlated with the ratio of fat/dry weight. In the only species in which comparisons were possible between newly emerged and swarming males (M. azurea), the former had significantly lower indices. Unmated females on average had lower wing wear indices than spent females. These facts suggest that wing wear reflects relative age.
3. The tandem males had significantly less wing wear than those in swarms, and are probably therefore younger. Age is therefore likely to be significant in relation to mating success.
4. Among males of the same relative age, tandem males had higher fat ratio than swarming ones, indicating that male mating success was also influenced by traits other than age. It is suggested that the shortest possible duration of the period of adult prematurity is adaptive, especially in insects with marginal adult food intake.     

Swarming behavior in male chironomid midges: a cost-benefit analysis

Aerial mating swarms of nonbiting male midges form at dusk andattract females from the surrounding vegetation. Females flyinto the swarm, and copulation occurs on the wing. Mating andpredation are identified as the major benefit and cost of swarmingand are influenced by swarm size in opposing ways. Swarms varygreatly in size but the individual's probability of mating isgreatest in the smallest swarms. However, the individual predationrisk is also greatest in the smallest swarms. These opposingeffects on swarm size combine in a common currency of matingsuccess per evening to favor males in the smallest swarms. Thereis also an effect of male body size. The smallest males occurpredominantly in the smallest swarms and have the highest matingsuccess. The mechanisms that might maintain the observed swarmsize distribution are discussed.     

Non-random Mating in the Dance Fly Empis borealis: The Importance of Male Choice

In the dance-fly Empis borealis (Diptera, Empididae), females form swarms to which males, carrying a nuptial gift, come for mating. We examined whether males or females were choosy and/or competed for mates. First, measurements of the size relationships between copulating males and females, nuptial gifts and the swarming females from different swarms were assessed. Second, male visiting time in differently sized female swarms was recorded. Larger (wing-length) females participated disproportionately in copulations in each swarm, but not for the population at large. Female mating status (virgin/non-virgin) or proximity to oviposition (egg size) did not influence the likelihood of copulation. No assortative mating pattern was found: male size and size of nuptial gift did not correlate with size of the mating female. The time spent by males in swarms increased with the number of females present and it took longer when males left a swarm without copulation than when doing so. Male visiting time per female was negatively correlated with number of females in swarms. Males more often left smaller than larger swarms without mating. We conclude that E. borealis males discriminate among females but find no evidence for male competition or for female choice. It is still a question to what degree females compete for males.     

Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host

Sex-role-reversed mating systems in which females compete for males and males may be choosy are usually associated with males investing more than females in offspring. We report that sex-role reversal may also be caused by selfish genetic elements which distort the sex ratio towards females. Some populations of the butterflies Acraea encedon and Acraea encedana are extremely female biased because over 90% of females are infected with a Wolbachia bacterium that is maternally inherited and kills male embryos. Many females in these populations are virgins suggesting that their reproductive success may be limited by access to males. These females form lekking swarms at landmarks in which females exhibit behaviours which we interpret as functioning to solicit matings from males. The hypothesis that female A. encedon swarm in order to mate is supported by the finding that, in release recapture experiments, mated females tend to leave the swarm while unmated females remained. This behaviour is a sex-role-reversed form of a common mating system in insects in which males form lekking swarms at landmarks and compete for females. Female lekking swarms are absent from less female-biased populations and here the butterflies are instead associated with resources in the form of the larval food plant.     

An alternative mating system in small male insects

Abstract. 1. Small males of all midge (Diptera: Chironomidae and Chaoboridae) species thus far examined (one chaoborid and six chironomids) are rare in mating swarms. They are found instead in vegetation adjacent to the swarm.
2. We show that it is here that females aggregate prior to embarking on mate acquisition flights. In the vegetation females appear to be accessible to males staying behind.
3. Such behaviour in small males may exploit the mate-attracting activities of large males in the swarm and may, at the same time, reduce competition and conserve energy.
4. The evolution and maintenance of these size-related types of mating behaviour are discussed.     

Why do males of the dance flyEmpis borealis refuse to mate? The importance of female age and size

Empis borealisfemales form swarms, and males carrying a nuptial gift come to swarms to mate. Males either mated with one of the females (accepted swarms) or left swarms without mating (refused swarms). Males mated with the younger (low wing-wear) and relatively larger females in accepted swarms. They seemed to be able to judge the relative size of the females but to ignore their absolute size. Visiting males stayed shorter in accepted swarms as female size variation increased. This probably reflects their greater ease in choosing a mate among females of relatively different sizes. Females in accepted swarms tended to be larger and to have less worn wings than females in rejected swarms.     

<Emphasis Type="Italic">Hilara</Emphasis> sp. (Diptera: Empididae; Empidinae): Mating System,Swarm Movements,and Inbreeding Avoidance

In a study spanning parts of nine years, an undescribed species of Hilara Meigen was observed to form mating swarms displaying complex behaviors. Typically, swarms were shaped like a flattened torus rotating rapidly about a horizontal axis. Many swarms also moved up and down and turned slowly back-and-forth about a vertical axis. Both up-and-down and turning movements were random in extent and direction, suggesting that they might arise as random, asymmetric density fluctuations within the swarms themselves. A rotating secondary swarm appeared intermittently inside one end of some primary swarms. Swarm membership changed continually as flies left one swarm to join another and as entire swarms coalesced. At one site the set of all swarms displayed properties not found in the swarms individually: spatial extension, daily dissipation and reconstitution over a period of weeks or months, reproductive potential, and gene flow. Such emergent properties qualify the set as a multicomponent swarm, an object heretofore known only in computer models. Hilara sp. appears to be protandrous, univoltine, and promiscuous. Generally, males paired preferentially with somewhat smaller females, but some small and medium-sized males paired with much larger females. Although males of nearly all known Hilara species present nuptial gifts of prey or other items to females, nuptial gifts were not observed at any time during the present study. Many characteristics of swarms of Hilara sp. can be understood as adaptations that reduce inbreeding.     

Widespread 'hilltopping' in Acraea butterflies and the origin of sex-role-reversed swarming in Acraea encedon and A. encedana

In some populations of the butterflies Acraea encedon and A. encedana, most females are infected with a bacterium that kills their sons. The resulting shortage of males is associated with females adopting a sex‐role‐reversed mating system, in which females swarm at landmarks such as hilltops and compete for males. We have observed the mating behaviour of Acraea species that are not known to be infected with the male‐killer. In over half of these species, males were found to aggregate on hilltops. It is likely that this behaviour was ancestral to the sex‐role‐reversed swarms of Acraea encedon and A. encedana, and we discuss how the spread of the male‐killing infection may have converted this mating system into sex‐role‐reversed swarming.     

Reproductive behavior and morphology of Paraleptophlebia spinosa (Ephemeroptera: Leptophlebiidae): implications of variation in copula duration

The reproductive behavior and genital morphology of a leptophlebiid mayfly Paraleptophlebia spinosa Ueno were studied in a population inhabiting a mountain stream in Kyoto, central Japan. Males formed swarms along gravel shores, caught females in the air, and mated on the ground. The distribution of the oviposition sites coincided with that of the swarming sites along the stream shore. The lobes of the male penis were characterized by a shallow pocket opening on the ventral side. The female vestibule formed a square-shaped chamber into which eggs were released from the oviducts. The number of eggs carried by females caught during copulation in the field showed a greater variation than the number of eggs of virgin females. Copula duration was strongly correlated with the number of eggs carried by the female. Significantly short copula duration with spent females (egg loading less than 20% of the estimated fecundity) may indicate that males could identify spent females. Copula duration with partially loaded females (egg loading between 20% and 80% of fecundity), however, was not shorter than that with fully loaded females. Male mating tactics with respect to copula duration and the possibility of kinematic sperm displacement are discussed with reference to the behavioral and morphological characteristics of the species. Received: September 3, 1999 / Accepted: December 9, 1999     

Relatedness and dispersal distance of eusocial bee males on mating swarms

Stingless bee males (Hymenoptera: Apidae) aggregate themselves for reproductive purposes. The knowledge of relatedness among the males attending the aggregations and the distance that they disperse from their natal nests to aggregations may provide important data to effectively conserve these bees. Here, we estimated these properties for Tetragonisca angustula (Latreille, 1811) males. Microsatellite molecular markers were used to genotype bees sampled from local nests and in mating swarms in order to identify the nests of origin of males and maternal genotypes of concerning queens. The distances from assigned nests to the mating swarms allowed us to estimate the distances travelled by males. A genetic relationship analysis was conducted to verify whether T. angustula males were closely related to nests where they aggregated. A pairwise relatedness analysis was also performed among all T. angustula males in each mating swarm. Our results demonstrated that T. angustula mating swarms received dozens to hundreds of males from several colonies (up to 70). Only two of the five mating swarms contained any males that were closely related to the bees from the new nests in construction. The relatedness among males was also extremely low. Yet, dispersal distance of T. angustula males ranged hundreds of meters up to 1.6 km, with evidence of reaching 2.25 km according to their flight radius obtained from their foraging area for locality. These data indicate a highly efficient mating system with minimal inbreeding in this bee species, with a great dispersal capability not previously found for stingless bee males.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.     

Avoiding Male Harassment: Wing‐Closing Reactions to Flying Individuals by Female Small Copper Butterflies

Males of many butterfly species persistently court and attempt to mate with females even if the females reject courtship. This male harassment almost certainly has negative effects on female fitness. Therefore, females have likely evolved strategies to avoid such encounters. To investigate the harassment avoidance strategy of females of the small copper butterfly, Lycaena phlaeas daimio, I observed the reactions of females to other individuals flying nearby in the field. In response to the conspecific butterflies, females closed their wings if they had previously been open and did not exhibit any action if the wings had been closed. Females that closed their open wings in response to a conspecific received fewer mating attempts than did females that held their wings open. These results indicate that the wing‐closing behaviour of L. phlaeas females functions to deter male mating attempts. The wing‐closing reaction occurred primarily in mated females. Because females of L. phlaeas copulate only once during their lives, this behaviour is not considered an indirect mate choice but rather an attempt to avoid persistent mating attempts (i.e. sexual harassment) by males.     

Swarm Site Fidelity in the Sex Role-Reversed Dance Fly Empis borealis

In the dance fly species Empis borealis (L.), females (1–40) gather to swarm at landmarks (swarm markers, like trees and bushes), and males carrying an insect prey visit these swarms for mating. We noticed earlier that some swarm sites were used for several years and that they appeared to be frequented by a similar number of swarming females in each year, although the numbers of females varied greatly among swarm sites and certain sites attracted more swarming individuals than others. To explore swarm site fidelity in this mating system, in 1993 we monitored the same swarm sites that we studied in 1989, addressing the questions, Would the same swarm sites still attract the same number of females and males after 4 years? and Why do some swarm sites attract more displaying females than others? The number of females swarming at the different markers in 1993 was approximately the same as 4 years earlier. Some of these swarm sites are known to have been used for 18 years. The swarm sites with the largest number of flies had a high sun exposure during the day and were found at coniferous swarm marker trees and in a mixed forest habitat. A swarm site with few females attending and with a low amount of insolation during the day can be predicted to be abandoned as a swarming site soon. Empis borealis swarm sites thus persist over many years and are attended by a similar number of individuals each year. To our knowledge, such site fidelity has not been demonstrated for any swarming insect species earlier.     

Contrasting sexual selection on males and females in a role-reversed swarming dance fly, Rhamphomyia longicauda Loew (Diptera: Empididae)

Although there are several hypotheses for sex-specific ornamentation, few studies have measured selection in both sexes. We compare sexual selection in male and female dance flies, Rhamphomyia longicauda (Diptera: Empididae). Swarming females display size-enhancing abdominal sacs, enlarged wings and decorated tibiae, and compete for nuptial gifts provided by males. Males preferentially approach large females, but the nature of selection and whether it is sex-specific are unknown. We found contrasting sexual selection for mating success on structures shared by males and females. In females, long wings and short tibiae were favoured, whereas males with short wings and long tibiae had a mating advantage. There was no assortative mating. Females occupying potentially advantageous swarm positions were large and, in contrast to selection for mating success, tended to have larger tibiae than those of rivals. We discuss our findings in the context of both the mating biology of dance flies, and the evolution of sexual dimorphism in general.     

Wing pigmentation in territorial male damselflies, Calopteryx haemorrhoidalis: a possible relation to sexual selection

One striking characteristic in adult males of some odonate species is the presence of wing pigmentation. In Calopteryx species, males show a series of pre- and postcopulatory behavioural displays during which they face females while showing their pigmented wings. One hypothesis to explain the precopulatory flying displays and the associated wing pigmentation is that they may serve a sexual selection function. I investigated this in the territorial damselfly Calopteryx haemorrhoidalis. Males of this species defend aquatic substrates that females use for oviposition. Observational evidence indicated that males with a higher proportion of wing pigmentation were more likely to defend a territory, obtained more matings, had fewer gut parasites, survived in the study site and stayed in territories for longer. Experimental evidence suggested that the relationship mating success and wing pigmentation still held when controlling for the size of the substrate defended by territorial males. Similar to other studies in the Calopterygidae, these results suggest that wing pigmentation may be favoured by sexual selection. I discuss, however, whether an alternative function for male copulatory courtship displays and wing pigmentation, as sexual and/or species recognition, may also explain the evolution of these traits. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.