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.     

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.     

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.     

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 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.     

Swarm behaviour and mate competition in mayflies (Ephemeroptera)

Although mayfly swarms are frequently cited as an example of lekking by insects, little is known about the behaviour of individuals within a swarm, or how mate-selection takes place. A study of five species of mayfly over a period of 10 consecutive years has revealed species-specific differences in the flight pattern of swarming males and in the ability of males to recognize swarms of their own species. Males of four of the five species jostle other males in the swarm at all times except when mating: mating pairs are not jostled. The pattern of jostling varies with the species. Measurements of the sperm content of the vesicula seminalis and of the wing length of members of individual swarms show that larger wing size is positively correlated with the presence of less sperm. The vesicula seminalis is always filled with sperm at the beginning of the imaginal stage and the testes regress before the beginning of the imaginal stage. If the volume of sperm in the vesicula seminalis is a valid index of mating success then males with larger wings have the highest success. Large wings may bestow an advantage during jostling. The males of Ephemera danica , which do not jostle, glide with outspread wings; these outspread wings may attract females, the largest wings being the most attractive. Females of all five species enter the swarm a few at a time, although many females may be resting beneath the swarm. This phased entry may decrease the attraction of the swarm for predators. The number of females in a swarm is not correlated with swarm size, and the factors which enable females to regulate their entry into a swarm remain obscure.     

Sexual selection in the gift-giving dance fly, Rhamphomyia sulcata, favors small males carrying small gifts

In some species of insects males transfer a gift to females during courtship or copulation. In the dance flies these nuptial gifts vary from nutritious prey items to inedible tokens such as a leaf, stone, or silk balloon. Nuptial gifts in dance flies are presumed to increase male mating success. We examined the strength and form of sexual selection on male Rhamphomyia sulcata, an empidid in which males provide females with a nutritious prey item as a nuptial gift. We found that whereas large males carried large gifts, neither large males nor gifts were targets of sexual selection. Indeed, correlational selection analysis and nonparametric examination of the fitness surfaces revealed that small males carrying small gifts were the most successful. Males may be more maneuverable or flight efficient with small gifts, or small males with large gifts may be unable to carry both a large gift and a female in the paired descent flight. These results suggest carrying constraints may be an important factor in determining selection on nuptial gift size. The largest target of sexual selection was old males. Old males were also paired with the largest and most fecund females, highlighting the role mate quality can further contribute to selection on males. Correlational selection analysis also revealed selection for an increase in covariance between male wing length and body size, and for an increase in slope between these traits. Males who deviate away from the optimal phenotypic relationship for two tightly related morphological traits, such as tibia and wing length, may have overall reduced performance. These findings highlight the role correlational sexual selection can play in optimizing nonsexual male morphology and scaling relationships. This study questions the role of the nuptial gift in dance flies as a resource for females.     

<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.     

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.     

Female reproductive decisions and parasite burden in a calopterygid damselfly (Insecta: Odonata)

There is currently a gap in sexual selection theory about how much the environment drives female mating decisions. We present field data that suggest that female sexual behaviour in the damselfly Calopteryx haemorrhoidalis is influenced by parasite burden. Male wing pigmentation in Calopteryx is a sexually selected trait that signals a male's ability to cope with eugregarine parasites (an intestinal parasite that feeds on the adult's ingested food). Because adult C. haemorrhoidalis females also show wing pigmentation, we examined whether this trait is similarly influenced by parasite burden and whether it may signal the female's reproductive value. MaleC. haemorrhoidalis defend riverine substrates that females use for oviposition. After copulation and during oviposition, females are guarded by the copulating male against intruder males. Alternatively, females may avoid mating and ‘steal’ an oviposition site within a male's territory. In the present study, we found that the amount of female wing pigmentation was negatively correlated with the number of eugregarines present. Females with more parasites produced fewer eggs, survived fewer days, spent less time during courtship, ‘inspected’ fewer males before mating, had a lower mating success, were guarded for less time during oviposition and engaged in fewer ‘stealing’ events during oviposition. The reduced egg production and survival of heavily infected females may result from eugregarine depletion of the females' consumed food reserves. Thus, to offset reduced longevity, heavily infected females may accept a mating more rapidly and mate with fewer males. ‘Stealing’ behaviour may be related to the female's differential use of sperm from some males, particularly high-quality males. Interestingly, males that mated with low-pigmented females showed greater variance in wing pigmentation than did males that mated with high-pigmented females. Possibly, female wing pigmentation may signal a female's reproductive value, which provides females with longer mate-guarding episodes and reduced interference from intruder males. This study points out one possible constraint, intestine parasites, that females may face during mating decisions. Because females in bad condition mate with males in both good and bad condition, this constraint may be pervasive enough to weaken the intensity of selection for a male sexually selected trait, wing pigmentation, and help to maintain its variation in phenotypic expression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

Courtship role reversal and deceptive signals in the long-tailed dance fly, Rhamphomyia longicauda

We examined the function of secondary sexual characters in the role-reversed, lekking behaviour of female long-tailed dance flies, Rhamphomyia longicauda Loew (Empididae), to test the hypothesis that the degree of abdominal distention is an honest female signal about the state of egg development. Female Rhamphomyia cannot hunt for prey and they receive all of their protein from males by exchanging copulations for nuptial prey gifts. Females compete for male gifts within leks that are organized for a brief period each evening before dark. Before hovering within leks, females swallow air, inflating expandable pouches on the pleural margins of the abdomen. The result is a large saucer-like abdomen which is further exaggerated by wrapping scaled pro-, meso- and metathoracic legs along its pleural margins. Male preference for an enlarged abdomen was confirmed by suspending plastic models of varying size from monofilament lines and recording which models attracted the most males. There was a positive relationship between egg development and abdominal distention in a related species, R. sociabilis (Williston), which lacks inflatable abdominal pouches. Multiple regression showed that in R. longicauda, abdominal inflation completely masks the state of egg development. We conclude that female R. longicauda deceive mate-seeking males with the unreliable message that eggs are nearing maturation in order to obtain a protein meal in exchange for copulation. Males that fail to identify a female bearing mature eggs risk near-certain cuckoldry and an increased probability that the female will die before oviposition. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sexual selection within mating swarms of the lovebug, Plecia nearctica (Diptera: Bibionidae)

Little is known about the structure of mating aggregations of insects or sexual selection within them. Male lovebugs (Plecia nearctica) hover in large swarms above emergence sites in the ground litter. Females emerge periodically and take flight through the hovering males. Females may be grasped by one or more males before or during flight. Male-male interactions and the structure of lovebug swarms are clearly related to competition for access to emerging females. Lovebug swarms are distinctly stratified vertically: large males at the bottom nearest the ground, medium-sized males in the middle, and small males at the top farthest from the ground. Large males closest to the ground have better access to females and experience greater copulatory success.     

Competition for access to mates predicts female-specific ornamentation and male investment in relative testis size

Sexually selected ornaments are highly variable and the factors that drive variation in ornament expression are not always clear. Rare instances of female-specific ornament evolution (such as in some dance fly species) are particularly puzzling. While some evidence suggests that such rare instances represent straightforward reversals of sexual selection intensity, the distinct nature of trade-offs between ornaments and offspring pose special constraints in females. To examine whether competition for access to mates generally favors heightened ornament expression, we built a phylogeny and conducted a comparative analysis of Empidinae dance fly taxa that display female-specific ornaments. We show that species with more female-biased operational sex ratios in lek-like mating swarms have greater female ornamentation, and in taxa with more ornate females, male relative testis investment is increased. These findings support the hypothesis that ornament diversity in dance flies depends on female receptivity to mates, which is associated with contests for nutritious nuptial gifts provided by males. Moreover, our results suggest that increases in female receptivity lead to higher levels of sperm competition among males. The incidence of both heightened premating sexual selection on females and postmating selection on males contradicts assertions that sex roles are straightforwardly reversed in dance flies.     

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.     

Swarming and mating of Aedes communis mosquitoes in nature

The date of the beginning of mating behaviour in males and females, the rate of insemination and the increasing of bloodsucking activity of females were studied in natural environments. Over 80% of females mated on the 3-4th day after emergence; after fertilization their behaviour changed from looking for males for coupling to looking for ones for a prey. The male swarming began on the 5th day after emergence and simultaneously the appearance of inseminated females was observed. The places of mating of males and females were investigated. It was established that coupling took place in swarms with swarming males and out of swarms with freely flying males.     

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.     

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.     

Nonlinear and correlational sexual selection on 'honest' female ornamentation

Female ornamentation has long been overlooked because of the greater prevalence of elaborate displays in males. However, the circumstances under which females would benefit from honestly signalling their quality are limited. Females are not expected to invest in ornamentation unless the fitness benefits of the ornament exceed those derived from investing the resources directly into offspring. It has been proposed that when females gain direct benefits from mating, females may instead be selected for ornamentation that deceives males about their reproductive state. In the empidid dance flies, males frequently provide nuptial gifts and it is usually only the female that is ornamented. Female traits in empidids, such as abdominal sacs and enlarged pinnate leg scales, have been proposed to 'deceive' males into matings by disguising egg maturity. We quantified sexual selection in the dance fly Rhamphomyia tarsata and found escalating, quadratic selection on pinnate scales and that pinnate scales honestly reflect female fecundity. Mated females had a larger total number and more mature eggs than unmated females, highlighting a potential benefit rather than a cost of male mate choice. We also show correlational selection on female pinnate scales and fecundity. Correlational selection, equivalent investment patterns or increased nutrition from nuptial gifts may all maintain honesty in female ornamentation.     

Sexual dimorphism in relation to swarming and pair formation patterns in leptocerid caddisflies (Trichoptera: Leptoceridae)

North European Leptoceridae (Trichoptera) perform three types of swarming flight patterns: (1) swarming males of Athripsodesand Ceracleafly in horizontal zigzag patterns over the water surface, (2) the Mystacidesspp. perform vertical zigzag movements, and (3) the flight of males of Triaenodes unanimisMcLach. is a mixture of the horizontal and vertical zigzagging. Also three groups of pair formation behavior can be distinguished. In the first group, of Athripsodesand Ceraclea,the females fly into the male swarms, where they are grasped and carried to the riparian vegetation by the flying males with the females hanging upside-down in genitalia coupling. In the second group, a Mystacidesfemale is caught by a male, when approaching a swarm and both use their wings to fly in tandem to the shore where they copulate. In the third group, of Triaenodes bicolor(Curt.) and Oecetis lacustris(Curt.), the males fly searching for females sitting on aquatic plants and when a female is found the male lands and they copulate immediately while clinging to the plant. The different swarming and mating behaviors might have favored selection for three types of sexual dimorphism: (1) longer forewings in males than females in species which fly in copula, (2) larger eyes in males of the vertically zigzagging species, and (3) much smaller males in the group where males search for females sitting on aquatic plants. In the second group approaching females are detected by males before reaching the swarm and in the third group the female almost always mates with the male which is the first to find her. In conclusion, we suggest that females of Athripsodesand Ceracleahave a greater choice among swarming males than do females of Mystacides, T. bicolor,and O. Lacustris.