Mating behaviour in the mosquito, Anopheles gambiae s.1.save

ABSTRACT. Mating behaviour in the Anopheles gambiae complex was studied in the laboratory, using an infra-red TV system to make observations in the 'dark'. Maximum fertilization occurred when both sexes were at least 2 days old. In LD 12:12 most mating took place in the first hour of the dark phase. At this time, the males had erect fibrillae on the antennae and showed the maximum response to an artificial female flight tone, approaching, landing-on and attempting to clasp the sound source. The cycle of fibrillar erection and of responsiveness to sound continued in constant dark. Males did not appear to discriminate on contact, between their own and other species. Previously mated females actively resisted copulation, but, when tethered, were unable to prevent the deposition of further internal mating plugs. Free-flying, previously inseminated, females prevented the males from depositing internal plugs, but not from ejaculating and depositing external plugs. The differences between A.gambiae and the better known Stegomyia mosquitoes appear to be related to their different habits, A.gambiae males being less likely to encounter females of other species or inseminated females of their own species at the restricted time and place of mating.     

Swarming and mating behaviour ofChironomus flaviplumus (Diptera: Chironomidae), compared with a sympatric congeneric species,C. yoshimatsui

The swarming and mating behaviour ofChironomus flaviplumus was observed and compared with a sympatric congeneric species,C. yoshimatsui. C. flaviplumus males swarmed around sunset near foliage or angles of buildings near the emergence site and copulated with females entering the swarm. Swarming and mating occurred under conditions of higher light intensity in cooler seasons than in warmer ones. Results suggested that temperature had an effect on the timing of flight to the swarming site in both sexes. TheC. flaviplumus swarm marker and swarming behaviour seemed very similar to that toC. yoshimatsui, and their respective daily swarming time zone greatly overlapped. No mixed swarm, however, was observed in the study area. This is probably due to the distance between the species' larval habitats. Possible premating isolation mechanisms between these 2 species are discussed.     

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.     

Mating alters the link between movement activity and pattern in the red flour beetle

Mating in arthropods is costly and has negative effects on survival. Such effects are often more strongly expressed when individuals are simultaneously exposed to other stress sources. Consequently, the behaviour of virgin and mated individuals often differs. Mated females, for example, search for suitable oviposition sites, whereas virgin females search more for mates. In the present study, we examine the effect of mating separately for females and males on four key behaviours of the red flour beetles: movement activity, movement along the edges of an arena, latency to emerge from shelter and preference for dark microhabitat. After mating, both sexes increase their activity at the same time as moving less along the arena edge, leading to a change in movement pattern. Females possibly change their movement pattern to locate suitable oviposition sites, whereas males perhaps do so to detect additional females with which to mate. Latency to emerge from shelter and dark preference are not influenced by mating, although they increase when measured again after 1 week. Of these behaviours, only movement activity is consistent at the individual level. We also examine whether mating incurs a cost as expressed in the time required to recover from a chill‐coma. The latter is a common proxy of cold tolerance in ectotherms. By contrast to our prediction, mating has no effect on chill‐coma recovery time, suggesting that either a single mating event does not incur sufficient stress or that there is possibly no trade‐off between the energetic cost of mating and of cold tolerance.     

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.     

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.     

Swarming behaviour of the mosquito Culex pipiens quinquefasciatus: a quantitative analysis

ABSTRACT. Analysis of video recordings of Culex pipiens quinquefasciatus Say swarms showed that the overall swarming patterns of males and virgin females are similar, even though the short-term characteristics of their flight, such as speed and turning angle, differ. This suggests they have the same response to the visual cue of the swarm 'marker'. The swarming pattern of an individual consists of elliptical loops which, in the short-term, define an area smaller than the swarm as a whole. The foci of these ellipses drift gradually with respect to the marker; individuals do not seem to have preferred positions within the swarm, but drift at random. Male mosquitoes identify and locate females by the sound of their wing-beats. Diffuse sound at the wing-beat frequency of female C.p. quinquefasciatus (500–600 Hz) caused males within the swarm to slow down significantly. Their turning behaviour remained unchanged, so the ellipses decreased in size. The swarm as a whole collapsed into a smaller volume, centred over the marker. Apparently, the response of males to sound consists of at least two parts: initially they alter their flight speed, and then alter their turning behaviour once they have located the source of the sound.     

Male roosting habits and mating behaviour of Myotis myotis

Attic-dwelling male Myotis myotis use different roost sites, but prefer one (or a few) of them and visit others sporadically. Roost-site preference can change, especially during the mating season. The males use their roost sites over years. Mean occupancy of all roost sites shows a maximum during the mating season. Females of different nursery colonies meet at male roost sites as far as 12 km from their colonies. They stay, on average, four days with one male, may join several males during one mating season and may visit their mating sites over years. Males appear to show no special behaviour to attract females but extend the time they are present at the roost site during the mating season. Each male is visited by about seven adult mates, on average. Differences in reproductive success are indicated by the times males were joined by females and by the numbers of mates and copulations. Two typical mating postures, copulation and five different social calls are described. Since females of different colonies meet at the male roost sites, the mating system of Myotis myotis may favour genetic exchange between colonies.     

Swarming and mating activity of Anopheles gambiae mosquitoes in semi‐field enclosures

Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is the major Afro‐tropical vector of malaria. Novel strategies proposed for the elimination and eradication of this mosquito vector are based on the use of genetic approaches, such as the sterile insect technique (SIT). These approaches rely on the ability of released males to mate with wild females, and depend on the application of effective protocols to assess the swarming and mating behaviours of laboratory‐reared insects prior to their release. The present study evaluated whether large semi‐field enclosures can be utilized to study the ability of males from a laboratory colony to respond to natural environmental stimuli and initiate normal mating behaviour. Laboratory‐reared males exhibited spatiotemporally consistent swarming behaviour within the study enclosures. Swarm initiation, peak and termination time closely tracked sunset. Comparable insemination rates were observed in females captured in copula in the semi‐field cages relative to females in small laboratory cages. Oviposition rates after blood feeding were also similar to those observed in laboratory settings. The data suggest that outdoor enclosures are suitable for studying swarming and mating in laboratory‐bred males in field‐like settings, providing an important reference for future studies aimed at assessing the comparative mating ability of strains for SIT and other vector control strategies.     

Call differences and calling site segregation in anuran species from central Amazonian floating meadows

Summary The acoustic behaviour of 15 sympatric and synchronically breeding species of frogs in an area of floating meadows near Manaus (Brazil) was studied for a period of 8 months. The calling positions of each species can be identified with certain physiognomic types of vegetation.Sound analyses were used to compare the mating calls. The main variables are dominant frequency, call duration and pulse repetition rate. Each of the 15 species has a distinct mating call and differs from the acoustic behaviour of each other one. Eleven species are separated in their dominant frequency ranges within their specific calling sites. Species sharing emphasised frequency ranges within identical calling sites differ greatly in at least two temporal variables.The roles of calling position, spectral, and temporal features of mating calls in species recognition and premating reproductive isolation are discussed.     

DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae

Anopheles gambiae populations in west Africa are complex, being composed of multiple, sympatric subpopulations. Recent studies have failed to reveal significant genetic differences among subpopulations, stimulating a debate regarding the levels of gene flow among them. The observed homogeneity may be the consequence of substantial contemporary gene flow or it may be that reproductive isolation is complete, but too recent for the accumulation of significant levels of genic divergence. Here, we report the results of a study estimating contemporary levels of gene flow between An. gambiae subpopulations by analysing females and transferred sperm removed from their reproductive systems. A total of 251 female and associated sperm extracts was analysed from a single site in Mali. Two molecular forms of An. gambiae, the M- and S-forms, occurred in sympatry at this site. Overall, we found very strong positive assortative mating within forms, however, we did observe significant hybridization between forms. In the M subpopulation 2/195 females (1.03%) contained sperm from S-form males and in 55 S-form females we found one female containing M-form sperm (1.82%). We also identified a mated M xS hybrid adult female. From mating frequencies, we estimate the Nem between the M- and S-form at 16.8, and from the adult hybrid frequency at 5.6. These values are consistent with our earlier estimate, based on FST for 21 microsatellite loci in which Nem = 5.8. We conclude that the general lack of genetic divergence between the M and S subpopulations of An. gambiae can be explained entirely by contemporary gene flow.     

The role of photoreception in the swarming behavior of the copepod Dioithona oculata

The copepod Dioithona oculata forms dense swarms near mangrove prop roots that are centered around shafts of light penetrating the mangrove canopy. Swarms can be created in the laboratory within light shafts created with a fiber optic light pipe. Laboratory observations of swarming behavior were recorded using video cameras, and the swimming behavior of the copepods and density of the swarms were quantified using video‐computer motion and image analysis techniques. Swarm formation results from a combination of phototactic and klino‐kinetic behavior. Dark adapted copepods initially exhibit a photophobic response to a light shaft, but become positively phototactic within 3–5 min after exposure to the light. Copepod aggregation rates under the light fit a saturation model, suggesting that copepods are attracted independently to the swarm marker. Copepods reverse their swimming direction when they encounter light intensity gradients near the edge of a light shaft, which aids in maintaining the swarm. Swarm formation can occur in the laboratory at light intensities as slow as 0.1 μM photons m^‐2 s^‐1, which is similar to light intensities at dawn when they are first observed to form in nature. Swarm formation appears to have an endogenous rhythm, as copepods will not form swarms at night under a light shaft.     

Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp

Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.     

Larvivorous capacity of Barbus pobeguini and possibility of using this in the fight against Anopheles gambiae s.l

Permanent breeding sites for Anopheles gambiae s.l. were found to occur in the urban area of Ouagadougou and to have some importance in the maintenance of vector populations. In these breeding places Barbus pobeguini was found widespread and larvivorous as indicated by the presence of remnants of A. gambiae in its stomach contents. The use of B. pobeguini would avoid the introduction of non-local larvivorous fishes. A series of trials carried out in laboratory conditions with B. pobeguini of different size, showed: 1) a remarkable capacity to ingest larvae (at different stages) of A. gambiae; 2) pronounced tendency by bigger B. pobeguini specimens to cope with bigger larvae; 3) an indifferent attraction to A. gambiae and Culex quinquefasciatus larvae.     

Behaviour, physiological states and thermal characteristics of aggregating male Hybomitra illota (Diptera: Tabanidae)

Male Hybomitra illota (Osten Sacken) were found aggregating in clearings in wooded areas in Rondeau Provincial Park, Ontario, Canada. At these sites they perched on a variety of substrates, and made frequent flights in pursuit of insects flying overhead. We know that these pursuit flights were part of the mating behaviour because some pursuits of female H. illota resulted in copulation. We call the aggregation sites 'mating arenas' and the behaviour exhibited by males 'perch-and-pursue'. Aggregation occurred only on sunny days, when ambient temperatures exceeded 18 degrees C. Males perched in sunny areas, except during hot afternoons, when some males were found in dappled shade. Some marked males remained at or returned to sites for up to 13 days, but most males did not remain at the same area within a site, even during the same day. The contents of the oesophageal diverticula of males were depleted daily. Concentration of diverticular carbohydrates changed through the season. Thoracic temperatures of males were high (c. 37 degrees C) and were regulated, probably both behaviourally and physiologically. The sites and behaviour of male H.illota at aggregation arenas bear some resemblance to lek sites and lekking in vertebrates. Males are aggregated in an arena but, within the perching component of the behaviour, we saw no evidence of male territoriality, display, or female choice. However, competition, display, or mate choice could occur within the pursuit-flight component.     

Large males have a mating advantage in a species of darter with smaller, allopaternal males Etheostoma olmstedi

Theory suggests that males that are larger than their competitors may have increased mating success, due to both greater competitive ability and increased attractiveness to females. We examined how male mating success varies with male size in the tessellated darter Etheostoma olmstedi. Previous work has shown that large males tend to move around and breed in vacant breeding sites, and consequently provide less care for their eggs, while smaller individuals can be allopaternal, caring for the eggs of other males as well as for their own. We studied female egg deposition in a natural breeding population using artificial breeding sites and in the laboratory, where female choice of spawning site was restricted to two breeding sites tended by two males of different sizes. In both the field and the laboratory, nests tended by larger males were more likely to receive new eggs. Additionally, the mean size of males associated with a nest was positively correlated with both the maximum coverage of eggs at the nest and the number of times new eggs were deposited. We discuss how the increased mating success of larger males, despite their decreased parental care, may help explain allopaternal care in this species [Current Zoology 56 (1): 1-5, 2010].     

Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae

Anopheles gambiae, the major malaria vector in Africa, can be divided into two subgroups based on genetic and ecological criteria. These two subgroups, termed the M and S molecular forms, are believed to be incipient species. Although they display differences in the ecological niches they occupy in the field, they are often sympatric and readily hybridize in the laboratory to produce viable and fertile offspring. Evidence for assortative mating in the field was recently reported, but the underlying mechanisms awaited discovery. We studied swarming behaviour of the molecular forms and investigated the role of swarm segregation in mediating assortative mating. Molecular identification of 1145 males collected from 68 swarms in Donéguébougou, Mali, over 2 years revealed a strict pattern of spatial segregation, resulting in almost exclusively monotypic swarms with respect to molecular form. We found evidence of clustering of swarms composed of individuals of a single molecular form within the village. Tethered M and S females were introduced into natural swarms of the M form to verify the existence of possible mate recognition operating within-swarm. Both M and S females were inseminated regardless of their form under these conditions, suggesting no within-mate recognition. We argue that our results provide evidence that swarm spatial segregation strongly contributes to reproductive isolation between the molecular forms in Mali. However this does not exclude the possibility of additional mate recognition operating across the range distribution of the forms. We discuss the importance of spatial segregation in the context of possible geographic variation in mechanisms of reproductive isolation.     

Cytonuclear Theory for Haplodiploid Species and X-Linked Genes. I. Hardy-Weinberg Dynamics and Continent-Island, Hybrid Zone Models

We develop models that describe the cytonuclear structure for either a cytoplasmic and nuclear marker in a haplodiploid species or a cytoplasmic and X-linked marker in a diploid species. Sex-specific disequilibrium statistics that summarize nonrandom cytonuclear associations in such systems are defined, and their basic Hardy-Weinberg dynamics and admixture formulae are delimited. We focus on the context of hybrid zones and develop continent-island models whereby individuals from two genetically differentiated source populations migrate into and mate within a single zone of admixture. We examine the effects of differential migration of the sexes, assortative mating by pure type females, and census time (relative to mating and migration), as well as special cases of random mating and migration subsumed under the general models. We show that pure type individuals and nonzero cytonuclear disequilibria can be maintained within a hybrid zone if there is continued migration from both source populations, and that females generally have a greater influence over these cytonuclear variables than males. The resulting theoretical framework can be used to estimate the rates of assortative mating and sex-specific gene flow in hybrid zones and other zones of admixture involving haplodiploid or sex-linked cytonuclear data.     

Laboratory colonization of Anopheles quadriannulatus from sympatry with other sibling species of the Anopheles gambiae complex in Zimbabwe

Abstract. A laboratory colony of the mosquito Anopheles quadriannulatus was established from a wild population occurring sympatrically with An.arabiensis in Zimbabwe. These sibling species are members of the An.gambiae Giles complex and were distinguished primarily by means of their specific polytene chromosome banding patterns. By using an ox-baited trap, we sampled selectively for the more zoophilic An.quadriannulatus. It was confirmed that An.quadriannulatus has the diagnostic slow allozyme of aspartate aminotransferase (AAT^95/95). In a mixed population under laboratory conditions, An.arabiensis displaced An.quadriannulatus within eight generations, without introgression. Colonization of An.quadriannulatus was facilitated by pooling the progeny from wild-caught mothers of confirmed identity and by using a specially adapted cage to promote mating.     

Courtship and mating behaviour of manta rays Mobula alfredi and M. birostris in the Maldives

The aim of this 14 year study was to elucidate the entire courtship and mating behaviour of manta rays Mobula alfredi and M. birostris using behavioural observations, video and photographic records. From 2003 to 2016, over 11,000 surveys were undertaken at known manta ray aggregation sites in the Maldives to record any observed manta rays reproductive activity. From 47,591 photo‐ID sightings, 4,247 individual M. alfredi were identified and 226 individual M. birostris from 229 photo‐ID sightings, all recorded at 22 atolls across 265 different sites. Courtship activity was observed on 206 surveys at 30 different sites. A total of 229 courtship events were recorded, with 90% (n = 205) of them occurring at cleaning sites. The observed courtship activity was categorised into seven distinct stages which are described in detail: initiation, endurance, evasion, pre‐copulatory positioning, copulation, post‐copulatory holding and separation. Photographs provide the first scientific record of the entirety of manta rays courtship and mating. Both M. alfredi and M. birostris appear to engage in the same elaborate courtship rituals, exhibiting the same behaviours during all stages of the courtship and mating process.