Genetic breeding system and investment patterns within nests of Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Dawson's burrowing bee is a large solitary ground-nesting bee endemic to the arid zone of Western Australia. In this study, we use microsatellite markers to analyse the genotypes of offspring from individual nests to determine the number of effective mates for each female. From these data we have determined that females almost certainly mate only once which is consistent with male reproductive tactics that include protandry and intense male-male competition for access to virgin females. We also use the molecular data to show that the nesting female is the mother of all the offspring of her nest and that brood parasitism is unlikely in this species. The data indicate that females make daughters at the beginning of the season followed by large sons in the middle, and then small sons at the end. Females often place one brood cell directly above another. The distribution of sex and morph in these doublets follows a pattern with most containing a female on the bottom and a minor male on the top, followed by almost equal numbers of female on top of female and minor male on top of major male. This pattern is likely favoured by emergence patterns, with males emerging before females and minor males emerging before major males. We suggest that although minor males have low reproductive success, their production may nonetheless be beneficial in that minor males open up emergence tunnels for their larger and reproductively more valuable siblings. In addition, minor males may be a best of a bad job product arising from changes in the costs to nesting females of gathering brood provisions over the course of the flight season.     

Seasonal change in offspring sex and size in Dawson's burrowing bees (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Abstract.  1. Nesting females of Dawson's burrowing bees, Amegilla dawsoni , produce a large size class of offspring, which includes daughters and major sons, and a small size class, which consists entirely of minor sons averaging half the weight of their larger siblings. Female allocation patterns change over the flight season such that the initial pattern of producing daughters shifts toward the production of both daughters and major sons in the middle of the season, and then the production of primarily minor sons in the latter part of the nesting season.
2. In Dawson's burrowing bees, this pattern is correlated with declines in pollen and nectar availability as the nesting season progresses as well as a heightened risk of dying before the final brood cell is completed. Here, the relation between these factors and the provisioning tactics of nesting Dawson's burrowing bees is discussed.     

Competition from large males and the alternative mating tactics of small males of dawson’s burrowing bee (Amegilla dawsoni) (apidae, apinae, anthophorini)

Males of Dawson’s burrowing bees (Amegilla dawsoni) search for virgin females at three locations: (1) open clay patches where females are emerging from underground brood cells, (2) the vegetated peripheral zone adjacent to emergence areas (through which females pass after emerging), and (3) clusters of flowering plants, which are often some distance from emergence areas. Males of Dawson’s burrowing bees exhibit a size dimorphism with large major and small minors. Major males patrol only the open emergence sites, whereas minor males may be found in all three locations. Although most females are mounted and presumably mated immediately upon emergence, some are not, and these females make up a pool of potential mates for the small males patrolling the peripheral zone and flower patches. The density of males at emergence sites and the probability of male-male aggression change over the course of a day and over the entire flight season. When the level of competition is low, some minor males hunt for mates at emergence areas, where potential mates are relatively numerous. But when the presence of many large rivals makes it unlikely that a small male can avoid being displaced from emerging females, minors make the best of a bad job by shifting to areas where majors are absent.     

Panmixia: an example from Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Dawson's burrowing bee is a large, fast-flying solitary nesting bee endemic to the arid zone of Western Australia. In this study the population structure of the species was examined with molecular markers. Using eight microsatellite loci, we genotyped 531 adult female bees collected from 13 populations of Dawson's burrowing bee, Amegilla dawsoni, across the species range. The mean number of alleles per locus ranged from 4 to 38 and expected heterozygosity was uniformly high with a mean of 0.602. Pairwise comparisons of F(ST) among all 13 populations ranged from 0.0071 to 0.0122 with only one significant estimate and an overall F(ST) of 0.001. The entire sample collection was in Hardy-Weinberg equilibrium and there was no evidence of inbreeding with a mean F(IS) of 0.010. The mating and nesting behaviour of this bee suggests that gene flow would be limited by monandry and the fact that almost 90% of females mate immediately on emergence. Nevertheless there is obviously sufficient gene flow to maintain panmixia, and we suggest that this results from infrequent and unreliable rainfall in the species range, which causes the bees to congregate at limited food resources, allowing a small number of unmated females from one emergence site to come into contact with males from another population. In addition, when drought eliminates food resources near an emergence site, the whole population may move elsewhere, increasing gene flow across the species range.     

Can minor males of Dawson's burrowing bee, Amegilla dawsoni (Hymenoptera: Anthophorini) compensate for reduced access to virgin females through sperm competition?

Dawson's burrowing bees (Amegilla dawsoni) exhibit a conditional mating strategy with two alternative tactics. Large (major)males exclusively patrol emergence sites in search of about-to-emergefemales, whereas small (minor) males usually search the peripheryof emergence sites for females that escape patrollers. About80% of the male population are minors, despite the fact thatpatrolling emergence sites is apparently the more profitablemating tactic. We tested the hypothesis that minor males gainfitness by mating with nonvirgin females and engaging in spermcompetition with rival ejaculates. If the sperm competitionhypothesis applied, it would help explain why nesting femalesproduce so many minor sons. Contrary to this hypothesis, however,we found that minor males do not exhibit traits frequentlyassociated with sperm competition. Minor and major males didnot differ in testis mass after controlling for body size.Neither did they differ significantly in the duration or patternof copulation nor in the volume of ejaculate transferred. Inaddition, and also contrary to the sperm competition hypothesis,females apparently mated only once. Loss of female sexual receptivityoccurred quickly after the onset of copulation, and nestingfemales appeared completely unreceptive. Thus, all aspectsof the bee's mating system strongly indicate that sperm competitiondoes not occur in Dawson's burrowing bee, so that minors cannotcompensate even partially via sperm competition for their mating disadvantage with virgin females.     

The Mating System of <Emphasis Type="Italic">Amegilla</Emphasis> (<Emphasis Type="Italic">Asarapoda</Emphasis>) <Emphasis Type="Italic">paracalva</Emphasis> Brooks (Hymenoptera: Apidae)

Males of the solitary bee Amegilla (Asarapoda) paracalva employ two mate-locating tactics: aggressive defense of sites from which virgin females are emerging and patrolling flower patches that are visited by conspecific females. At one study site, a single male was able to control an entire emergence area for one or more days. Multiple males patrolled one flower patch, interacting aggressively on occasion but no one individual was able to monopolize this resource. Territorial males at the emergence site secured mates by waiting by tunnels for receptive virgin females to emerge after metamorphosis. Males patrolling the flower patch pounced upon flower visiting conspecifics and mated with receptive females there. Territorial males at the emergence site were larger than average individuals, probably because of the advantage larger males have when grappling with opponents. Flower patrolling males were smaller than territorial males at the emergence sites, perhaps because of the advantages gained by these males from rapid, agile flight.     

Male size and survival: the effects of male combat and bird predation in Dawson's burrowing bees, Amegilladawsoni

1. Males of Dawson's burrowing bee, Amegilla dawsoni , occur in two size classes, large majors and small minors. Major males compete aggressively for emerging females in completely exposed emergence areas, whereas minors often employ an alternative mating tactic, which involves rapid patrolling in the vegetated periphery of emergence areas.
2. Because major males wrestle violently with rivals on the ground, they experience greater wing wear and a higher risk of wing damage than minor males. In addition, males patrolling emergence areas and waiting on the ground for emerging females are more likely to be killed by predatory birds than are peripheral minors.
3. Measurements of longevity based on mark–recapture data suggest that majors are slightly shorter-lived than minor males. If male–male combat and predators do reduce the lifespan of major males relative to minors, the effect would be to decrease the lifetime mating advantage of majors relative to minors.
4. Differential mortality could therefore be a factor in the maintenance of the two forms of males in this species.     

The relation between male body size, fighting, and mating success in Dawson's burrowing bee, Amegilla dawsoni (Apidae, Apinae, Anthophorini)

Males of the bee Amegilla dawsoni (Anthophorini) vary greatly in size, with some of the largest individuals as large as the largest females, a rare phenomenon in insects. The occurrence of unusually large males appears to be the product of sexual selection for fighting ability. As predicted from this hypothesis: (1) males regularly competed aggressively to be in the best position to mount sexually receptive, virgin females as they emerged from the ground; (2) larger males usually won fights for potential mates, as demonstrated by the fact that males able to defend sites with an emerging female were larger on average than males they kept at bay; (3) the fighting advantage of large males translated into greater mating success. Males captured while mounted on a female were significantly larger on average than randomly captured matesearching males in two of three populations sampled in 1993. Moreover, males known to mate more than once were consistently larger than single-mating males in the 10 samples taken from four populations examined in 1994. Thus, a large male mating advantage applies across years and among populations, making it potentially advantageous for females of Dawson's burrowing bees to produce large, superior fighting sons about the same size as their daughters.     

Female mating success and risk of pre-reproductive death in a protandrous grasshopper

Numerous studies have assessed the adaptive value of protandry for males in several insect species, considering that male emergence is determined by female availability. However, the possible advantage of the time of emergence for females on their mating success in protandrous insect species has only been explored theoretically. By studying the grasshopper Sphenarium purpurascens we evaluated the hypothesis that late emergence could be adaptive for females. If female maturation occurs when the population density is higher and the sex ratio (males/females) is biased to males, their probability of mating increases. Thus, in this study we estimated (1) the opportunity for mating in females as a function of their sexual maturation time, population density, and sex ratio at the moment they reached sexual maturity. In addition, (2) an analysis incorporating female body size and the total number of female matings was performed. Both analyses support the occurrence of protandry in the studied population. Under the first approach, females with intermediate maturation time had a higher probability of being mated than earlier and late matured females. Thus, it suggests that stabilising selection is acting on female maturation time and this may affect selection on male maturation time. Furthermore, the proportion of mated females increased when the sex ratio was biased to males, and stabilising selection on maturation time was detected also. However, the number of matings of a female depended on her body size. Females with larger body size had more matings than smaller ones at the beginning of the reproductive season. Because selection acts differently on maturation time in males and females of S. purpurascens this result is consistent with a condition for the maintenance of protandry in the population. The present results are discussed in the light of the models for the evolution of protandry.     

Impact of the Timing of Male Emergence on Mating Capacity of Males in Trichogramma evanescens Westwood

In species with highly structured population, such as Trichogramma spp., mating occurs mostly at emergence on the patch and early emerging males have an advantage, as they are present when the first females emerge. However, early emergence of male could also enable males to mature sexually before the emergence of females or enhance their capacity to induce higher receptivity in females. We measured time of emergence of male and female Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) from hosts that were parasitized within a 30 min period. We also measured the effect of male age on their capacity to mate, and the ability of inseminated females to produce daughters. To verify if early emerging males induced higher receptivity in females, we observed the females mate choice between males of different ages. Our results indicated that the mean time of emergence between males and females was 29 min for individuals that develop in 9 days and 10 min for individuals that develop in 10 days. The protandry observed in this species could be the result of either a faster development of males or a male first strategy by the ovipositing female. In T. evanescens, protandry does not permit males to mature sexually nor to induce higher receptivity in females. The main advantage of protandry for males thus appears to be early access to females as they emerge.     

Male emergence timing and mating success in the funnel-web spider,Agelena limbata (Araneae: Agelenidae)

Field observations on the relationship between male mating success and emergence timing in the funnel-web spider,Agelena limbata, were conducted.Agelena limbata is an annual species and adult males appear slightly earlier than adult females in July. As males deposit a copulatory plug at the female epigynum after copulation, copulation with virgin females is important to males. The number of copulations in males with virgin females, which strongly correlates with the longevity of males and the number of females that males courted, did not correlate with the emergence timing of males. Early emerged males and females were significantly larger in size than later ones, but the correlation coefficient between the emerged date and the cephalothorax width was not strong. Males that emerged earlier did not have any advantage in copulating with larger and more fecund females. Furthermore, virgin females first copulated on average 7.9 days after their final molt and the mortality rate of adult males increased after the final molt. These factors may favor the smaller degree of protandry in male emergence timing inA. limbata.     

A SEX DIFFERENCE IN THE PROPENSITY TO ENTER DIRECT/DIAPAUSE DEVELOPMENT: A RESULT OF SELECTION FOR PROTANDRY

In monandrous mating systems with discrete nonoverlapping generations males should maximize the expected number of matings by starting to emerge before females. This is known as protandry. Moreover, Evolutionarily Stable Strategies (ESS) models show that the male emergence curve should be abruptly truncated before female emergence has ceased. In temperate areas where many insects have partial second generations, we accordingly predict that males should enter diapause development at an earlier date than should females, as a result of late-emerging males being penalized in terms of fewer mating opportunities. The decision to diapause or to develop directly is usually mediated by response to environmental stimuli of which day length is the most important. Hence we predict that the mechanism by which males enter diapause at an earlier date than females will be that of the male reaction norm for diapause development being shifted towards longer day lengths when compared to that of females. As a result of the greater tendency of males to enter diapause development, partial second generations that develop directly should be female biased. As a corollary, first generations should be male biased because some males of the first generation are from the previous year. The prediction that males should enter diapause development earlier in the season, i.e., at longer day lengths, as compared to females was corroborated by rearing Pieris napi under a variety of critical day length regimes producing mixed broods of directly developing and diapausing individuals, and by outdoor rearings of cohorts of larvae of P. napi and P. rapae initiated throughout the season. The prediction that partial second generations should be female biased was corroborated by laboratory rearings at constant temperature of P. napi (Pieridae), Polygonia c-album (Nymphalidae), and Pararge aegeria (Satyridae) under critical day length conditions, producing female-biased sex ratio under direct, and male-biased sex ratio under diapause development.     

Models for the evolution of protandry in insects

Protandry is the tendency for males to emerge before females, and it is common in insects with discrete, nonoverlapping generations in which females mate once only soon after emergence. In these circumstances males which emerge early will have more opportunities to mate than those which emerge late, so that protandry would be expected to evolve through sexual selection. In diploid species in which the primary sex ratio is fixed, protandry can evolve only through shortening the developmental time of males, so changing the distribution of their emergence times. Two models of the evolution of protandry in this way are compared. The first model assumes that the distribution of male emergence times can respond without any constraint to sexual selection, so leading to an “ideal free” distribution; the second model assumes that the distribution can shift only in mean (or possibly in mean and variance), but not in shape.     

Why do males emerge before females?

Summary In butterflies and many other insects there is a general tendency for males to emerge before females. This is known as protandry. In this paper we advance the hypothesis that protandry is a reproductive strategy of males, resulting from competition for mates, and should primarily occur in species maintaining female monogamy. Our hypothesis is corroborated by applying a mathematical treatment to a theoretical population with seven defined properties, all of which are argued to be reasonable assumptions for natural populations.     

Protandry in the parasitoidCardiochiles nigriceps,as related to its mating system

A laboratory study was conducted of the emergence times and mating success ofCardiochiles nigriceps Viereck (Hymenoptera: Braconidae), a larval parasitoid of the tobacco budworm,Heliothis virescens (F.) (Lepidoptera: Noctuidae), and in view of this information, the parasitoid's mating system was explored. Observations on laboratory populations ofC. nigriceps confirmed the occurrence of two types of protandry, i.e. seasonal and diurnal; males emerged 2 days before females in a generation, and emerged about 1 hr before females on a given day. An experiment on mating success showed that newly emerged females are not receptive to males that emerged 1 hr earlier, but that these males and females often mate successfully after 1 more hr. The experiment also showed that 1- to 5-day-old males are more successful than 1-hr-old males in mating with 0- to 1-hr-old females. Thus, it is argued that males emerging on a given day have a disadvantage in competition for mates with males that emerged days earlier, and that this disadvantage may serve as a selection pressure toward diurnal protandry. A monogamous mating system for females ofC. nigriceps is suggested because sexual selection would be expected to be strong in species exhibiting both seasonal and diurnal protandry. A possibility of a sibling mating system inC. nigriceps is questioned partly because newly emerged females are unreceptive to males that emerged 1 hr earlier and partly because this parasitoid is solitary in what is considered highly dispersed hosts in the field.     

Agonistic behaviour of age 0, age 1 and non-breeding adult Arctic grayling Thymallus arcticus (Pallas)

Age 0 Arctic grayling begin to show agonistic behaviour 3 weeks after emergence and are territorial by their fourth week. Age 1 fish are territorial throughout the summer feeding period. In adults, territoriality is restricted to larger males during the early spring breeding season while after the breeding season both smaller adult males and adult females also hold territories.
In sub-adults, larger fish and resident fish tend to win most fights. In adults, males usually win against females. In fights between adults of the same sex, larger and resident fish usually win.
The lateral display becomes more important in the agonistic repertoire of Arctic grayling as they mature and the characteristic large dorsal fin develops. Arctic grayling appear to lack an appeasement display.     

Sex‐related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the ‘rank advantage’ and the ‘differential susceptibility’ hypotheses, nor the ‘mate opportunity’ hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with ‘mate choice’ arguments, whereby females use condition‐dependent arrival date to assess mate quality.     

Emergence patterns in male butterflies: A hypothesis and a test

A game theoretical model is advanced to explain the emergence time schedule of male butterflies under temporal “apostatic” selection, so that males emerging on different days enjoy equal fitness in evolutionary equilibrium. The model predicts not only the position of the peak date but also the shape of the male emergence curve for any given female emergence schedule. Where the female emergence curve is smooth with one peak, a flight season can be divided into an earlier phase, when some males emerge every day, and a later phase in which no male emerges. The male emergence curve is truncated at the boundary of the phases. The position of the truncation point is determined by the difference between pre- and postemergence mortality. Preemergence mortality also determines the rate coefficient of the decrease in sex ratio through the season. The model is applied to a well-studied population of the butterfly Euphydryas editha. The male presence curve fits well, but no clear truncation exists in male emergence, and some males emerge earlier than predicted. Reasons for deviations are discussed.     

Phenology of two territorial solitary bees, Anthidium manicatum and A. florentinum (Hymenoptera: Megachilidae)

Five years' data on phenology of an Anthidium manicatum population in southern Germany and comparative observations on A. manicatum and A. florentinum from southern France are analysed. Males and females had the same flight season, adult sex ratio was strongly female biased and males were larger than females in both species. This is the opposite pattern to most other solitary bees, where females generally are larger than males, sex ratio is male-biased, males emerge before females and males disappear long before females. We argue that two features of Anthidium female behaviour, namely prolonged sexual receptivity and use of resources easily defendable by males, explain male adaptations in behaviour, phenology and body size and, hence, population sex ratio.     

Can relaxed time constraints on sperm production eliminate protandry in an ectotherm?

In most temperate-zone reptiles, as in many other ectothermic taxa, males emerge from periods of inactivity (e.g. hibernation) before females, a pattern referred to as protandry. In the large body of theory depicting its evolution it is assumed that as selection pressures on females moderate female emergence time, net sexual selection on males shifts male emergence time accordingly. This is because early-emerging males might (i) benefit from advantages in behavioural interactions (e.g. obtain more matings, better territories, or a higher social status), or (ii) produce and mature more spermatozoa before the mating season. These putative advantages of early emergence occur simultaneously in most temperate-zone reptile species, because sperm production and copulations occur soon after emergence from winter inactivity. Thus, it is difficult to distinguish between the two hypotheses. To do so would require a system in which behavioural interactions occur at one time of year and sperm production at another. The southern snow skink ( Niveoscincus microlepidotum ) provides such an example; adult males fight with each other immediately after emerging from hibernation, but examination of the testes and epididymes of males throughout the year show that males do not produce spermatozoa until around 3 months later. Thus, the 'behavioural interactions' hypothesis predicts protandry in snow skinks, whereas the 'sperm production' hypothesis predicts synchronous spring emergence in males and females. Our field data, collected over 5 years, show that emergence dates in spring are the same for male and female skinks. Hence, when the selection pressure for rapid sperm production is relaxed, we no longer see the protandric emergence pattern characteristic of most temperate-zone reptiles.