Mating Flight Research Articles

Molecular Population Genetics of Social Insects

The life of social insects centers around sedentary colonies that can include individuals belonging to different patrilines or matrilines, with a turnover of reproductives. The colony is a scene for both cooperation and conflicts, and the conceptual framework for the evolution of social life and colony organization is provided by the kin selection theory. Variable molecular markers make it possible to dissect kinship within colonies, identifying patrilines and matrilines and estimating genetic relatednesses. Such markers have been used to test hypotheses on social conflicts between queens and workers (split sex ratio hypothesis), among workers (worker policing hypothesis), and among reproductive females (skew hypothesis). The data from several species of ants, bees, and wasps indicate that workers can obtain information on the genetic heterogeneity of their colonies and use that information to manipulate reproductive decisions. The social structure of colonies and the mode of colony founding affect the population-wide dispersal of sexuals. Populations with multi-queen colonial networks have limited dispersal; females stay in their natal colonies, and mating flights can be restricted. As a result, coexisting queens tend to be related to each other, maintaining the genetic integrity of colonies, and populations become spatially differentiated to an extent that can lead even to socially driven speciation.

Source of alate excitant pheromones in the red imported fire antSolenopsis invicta (Hymenoptera: Formicidae)

At the onset of mating flights inSolenopsis invicta, workers swarm excitedly over the mound as alates prepare to fly. Previous studies demonstrated that this excitement is stimulated by the male and female alates. We investigated the glandular source(s) of pheromones produced by the alates that cause excitement. The only common female and male alate body part that elicited excitement when crushed was the head. Within the head, excised mandibular glands were found to be responsible for worker excitement. Fire ant workers are very sensitive to external stimuli and some excitement was elicited by crushed female gasters and male thoraces, but the response was never as significant as with crushed heads. Tests with summer and winter alates revealed similar results, except that gasters of winter female alates had a greater excitant effect than did gasters of summer female alates. This may be due to the production of attractant pheromones by the poison glands of overwintering female alates. We conclude that the mandibular gland is the source of alate excitant pheromones.

Laboratory observations of nuptial flights of the ant Polyrhachis laboriosa.

Ethology of Polyrhachis laboriosa, an ant species from equatorial Africa, is little known. No field observation of a nuptial flight of these ants was ever made. We describe two nuptial flights observed in a laboratory colony of P. laboriosa at a 3 days interval. They both occurred in the morning while the nest was kept in near darkness (less than 2 lux of daylight). Flying activity of the alates was suppressed within 1 h by their exposure to daylight of about 140 lux, and within several minutes by their exposure to a lamp emitting white light of 3,000 lux and acting as a source of heat. On the day following the first flight the alates and the workers showed exceptionally high level of mutual grooming. The alates, in particular the males, were transported by workers to the brood chambers whenever they strayed outside and after the nuptial flights.

MICROSATELLITES REVEAL HIGH POPULATION VISCOSITY AND LIMITED DISPERSAL IN THE ANT FORMICA PARALUGUBRIS.

We used microsatellites to study the fine-scale genetic structure of a highly polygynous and largely unicolonial population of the ant Formica paralugubris. Genetic data indicate that long-distance gene flow between established nests is limited and new queens are primarily recruited from within their natal nest. Most matings occur between nestmates and are random at this level. In the center of the study area, budding and permanent connections between nests result in strong population viscosity, with close nests being more similar genetically than distant nests. In contrast, nests located outside of this supercolony show no isolation by distance, suggesting that they have been initiated by queens that participated in mating flights rather than by budding from nearby nests in our sample population. Recruitment of nestmates as new reproductive individuals and population viscosity in the supercolony increase genetic differentiation between nests. This in turn inflates relatedness estimates among worker nestmates (r = 0.17) above what is due to close pedigree links. Local spatial genetic differentiation may favor the maintenance of altruism when workers raise queens that will disperse on foot and compete with less related queens from neighboring nests or disperse on the wing and compete with unrelated queens.

Neighborhood density and reproductive potential in harvester ants

When neighbors compete for resources, the characteristics of a neighborhood may affect fitness. We examined the relationship between reproductive success and the density and size/age characteristics of neighbors in a population of the seed-eating ant, Pogonomyrmex barbatus, in which the ages of all colonies were known. Reproductive success was estimated by trapping and counting the number of alate, reproductive ants emerging from the nest for the annual mating flight. Alate production was negatively related to neighborhood density. Decreased production of alates by more crowded colonies may be due to competition for food with surrounding colonies. Neighbor size/age was unrelated to alate production. If alate production is correlated with lifetime reproductive success, these results suggest that selection favors colonies that monopolize more space, whatever the size of neighboring colonies.

Ontogeny of cephalic volatile patterns in queens and mating biology of the neotropical stingless bee, Scaptotrigona postica

Summary Chemical communication is an ancient yet still immensely important part of reproduction. Amongst all invertebrates, the most sophisticated “chemical languages” are used by social insects. Here the sex- and caste-specific pheromonal messages consist of multicomponent mixtures. In the neotropical stingless bee Scaptotrigona postica, an inhabitant of dense tropical rain forests, the cephalic volatiles of a queen transmit information on her reproductive status to males. A distinct ontogenetic pattern of the queen pheromone composition allows drones to discriminate receptive virgins which are then chased during the short nuptial flight through the forest understorey. By means of gas chromatographic/mass spectroscopic analyses, the numerous volatile compounds found in pentane extracts of individual bee heads could be identified. Qualitative as well as quantitative changes of these volatiles in the course of imaginal development could be determined, and bioassays with synthetic compounds were undertaken in order to decode the chemical signals used during the short encounter of a young queen and her mate.

Intraspecific interactions in a community of arboreal nesting termites (Isoptera: Termitidae)

In coconut plantations of northern New Guinea, the arboreal nesting termite community comprises three species:Nasutitermes princeps, N. novarumhebridarum, andMicrocerotermes biroi. In orde to assess the importance of intraspecific interactions in this community, we conducted pairwise encounters between batches of individuals in the laboratory and between entire nest populations in seminantural conditions. Three levels of agonism were defined in laboratory bioassays: anagonism, moderate agonism, and strong agonism. Anagonism was observed during all control tests with homocolonical groups and in some tests with allocolonial groups of all species. Moderate agonism included initial aggressiveness that subsequently faded out, and initially passive encounters where aggression progressively built up and led to fighting. Strong agonism corresponded to initial aggressiveness and fighting. Results obtained in alboratory bioassays were consistent with bioassays in seminatural conditions. WhenNasutitermes colonies were anagonists in laboratory bioassays, their foraging trails merged without aggression in field tests.N. princeps nests that were moderately agonistic in laboratory tests fought and either continued to avoid each other or finally joined after elimination of the most aggressive individuals. The most aggressiveM. biroi andN. princeps colonies fought and their foraging trails diverged afterward. Direct attacks on alien nests were winnessed inM. biroi. In all species, anagonism occurred in 21–34% of the combinations tested, between either geographically close or distantcolonies. An exeption was a group of 112 anagonist nests ofN. princeps, which most probably constituted a supercolony. The level of agonism betweenNasutitermes colonies was constant during the wet and dry season. Termite colonies excluded each other, both intra- and interspecifically, from the coconut trees, and their territories seem distributed in a mosaic pattern. Agonism between colonies may result in the elimination of the weakest colonies or in trail divergence, maintaining this mosaic. In cotrast, lack of agonism between some colonies suggests the possibility of colony fusion and gene exchanges without nuptial flights.

Behavioural and ecological aspects of nuptial flights of the termitophilous phorids Termitophilomyia zimbraunsi and Mesopathusa modesta (Diptera: Phoridae) in Zimbabwe

Nuptial flights of Termitophilomyia zimbraunsi were observed over three years (1990‐1993) near the open chimney of an Odontotermes transvaalensis mound in Harare, Zimbabwe. Copulating phoretic pairs landed on the chimney; males quickly disengaged and flew away whilst females ran inside the vent and tore off their wing membranes. Agitated termite workers and soldiers swarmed the rim in a partially successful physical attempt to expel the phorids; the termites appeared to anticipate the threat of invasion. After acquiring the scent of the nest, female phorids ran underground to lay their large single eggs, probably in the hosts’fungus gardens. Nuptial flights occurred throughout the year but only in the early mornings, peaking in the hot dry season and being least in the hot wet season. The flights were highly temperature dependent (15.0‐17.9 °), usually occurring at relatively low light intensities but across a wide range of humidities. Phoresy and sexual dimorphism in wings, mouthparts, food and division of labour in T. zimbraunsi are discussed, as is its termitophilous habit and the responses of termites to it.Although the females of Mesopathusa modesta are apterous, nuptial flight behaviour is very similar to that of T. zimbraunsi. Neither phorid is host‐specific, both species having been found on both Odontotermes latericius and O. transvaalensis mounds, although M. modesta is more common on O. latericius mounds.

Reproductive mechanisms and dynamics of habitat colonization inMicrocerotermes biroi(Isoptera: Termitidae)

Abstract.1. Previous studies on the arboreal termite community in coconut plantations of northern New Guinea showed thatMicrocerotermes biroiis the most abundant species, despite the fighting superiority of two competitor speciesNasutitermes princepsandN.novarumhebridarum.In this study we tested the hypothesis that the success ofM.biroiis due to its efficiency at colonizing new habitats following nuptial flights.2. We demonstrated experimentally the ability ofM.biroicolonies to replace their reproductives when removed, or to produce reproductives in satellite nests when isolated from the remainder of the colony. Replacement reproductives were always neotenics, derived from nymphs or workers.3. Despite the ability of neotenics to differentiate within their home colonies, 84% of field colonies were headed by dealated imagos. This value constitutes a minimum estimate of the proportion of field colonies founded independently by imagos after the nuptial flight.4. The monitoring of a young plantation during the first 31/2 years of its colonization by arboreal nesting termites revealed its invasion byM.biroi, which colonized 63% of the trees while neitherNasutitermesspecies appeared.5. Our results demonstrate thatM.biroiis actually a pioneer species, able to invade a new habitat by means of nuptial flights. They outline the importance of each species' reproductive strategy in shaping the arboreal‐nesting termite community.

Succession, Forest Fragmentation, and the Distribution of Wood Ants

I tested the hypothesis that the distribution of territorial wood-ant species (Formica rufa group) of different colony structure and dispersal strategy relate differently to the dynamics and landscape structure of boreal forests. Monogynous species (colonies have only one queen and inhabit one nest) that disperse through nuptial flight and subsequent temporary nest parasitism, should primarily be found in young forests and in smaller old-forest fragments. These long-distance dispersers can reach these areas where the nests of F. fusca group ants (which the wood-ant queens invade and parasitize) are more common, and these wood-ant colonies can monopolize the small fragments. Polygynous species (colonies have many queens) that disperse mainly through nest budding and may form large colonies of cooperative nests, should primarily be found in old forests and larger old-forest fragments. In such patches these short-distance dispersers have enough space for developing into strong colonies capable of ruling out all other territorial species. I mapped the nests of eight territorial ant species, three of which belonged to the wood-ant group, in fragmented forests of different age in southern Finland. In general, the mapping data supported my hypotheses. The monogynous F. lugubris was more common in young forests and in small old-forest fragments than expected by chance. The polygynous F. aquilonia was more common in old forests and in larger old-forest fragments.

Mermithid Nematode Parasitism of Solenopsis Ants (Hymenoptera: Formicidae) of Northern Florida

Sexuals collected from nests of the fire ant, Solenopsis geminata (F.), the red imported fire ant, S. invicta Buren, and S. pergandei Forel in the Apalachicola National Forest were parasitized occasionally by a large mermithid nematode. Summer infection rates (1991–1993) varied by species and sex: 0% for S. invicta gynes, between 1 and 7% for S. pergandei gynes and males of all 3 species, and 16% for S. geminata gynes. The seasonality of infection coincided with the summer reproductive period of S. geminata and suggests the mermithid has an annual life cycle. The parasites, up to 15.5 cm in length, distend the abdomen of the host, but have little anatomical effect other than detracting from sex organ development. Mermithisized ants do not participate in mating flights and die when the parasites emerge. The mermithids emerge as sexually immature larvae, precluding their identification or taxonomic description. A mermithid this large has not been reported previously in Solenopsis . Currently, there is no record of mermithid parasitism in S. invicta and S. pergandei nor have mermithisized sexuals been reported in the genus.

The rhythms of sperm release from testis and mating flight are not correlated in Lymantria moths

The circadian rhythm of the release of sperm from the testes into the vasa deferentia in wild gypsy moth (Lymantria dispar) males was found to be the same as the rhythm previously observed in the laboratory strain of the same species. To determine the temporal relationship between sperm release and mating activity, daily rhythms of sperm release and mating flight were compared in two closely related species, L. dispar and L. monacha. While the peaks of sexual activity of wild males were approx. 8 h apart, the period of sperm release was essentially identical in the two species. It was concluded that the phase of sperm release is not linked to the phase of mating activity but rather, the two rhythms are independently timed.

Storage proteins in ants during development and colony founding

Three classes of storage proteins from larvae of four species of ants ( Crematogaster opuntiae, Pheidole spadonia, Solenopsis xyloni and Conomyrma sp.) were identified and characterized for native and subunit sizes, density and amino acid composition. First, hexamerins contained moderately high proportions of aromatic amino acids ( x ̄ = 12.9 mol% ). A second type of storage protein contained extremely high proportions of glutamine/glutamic acid ( x ̄ = 21.1 mol% ). Third, dimeric proteins had densities suggesting they were very high density lipoproteins (VHDL). These VHDLs may be homologous with similar proteins that carry chromophores in Lepidoptera. The same types of storage proteins found in larvae were also present in the fat bodies of adult queens at the time of their mating flights. The class of the dominant protein varied with species. In Cr. opuntiae queens, storage proteins were almost completely depleted during colony founding. In ants, the ability of adult females to express storage protein genes may have been an important step in the evolution of the claustral mode of colony initiation, in which females can produce the first set of workers without leaving the nest to search of food.

Reproductive behavior of the antLeptothorax (Dichothorax) pergandei

Leptothorax pergandei, the only member of the subgenusDichothorax, is a common ant in Chihuahuan desert habitats in southwestern Arizona. According to colony censuses and relatedness estimates, colonies are mostly monogynous and queens typically mate only once. Mating takes place in local swarming flights; virgin queens attract males with secretions from the poison gland. Some dealate queens running on the soil surface directly after the mating flight had well-developed ovaries containing mature eggs and yellow bodies.

Colony founding by queen association and determinants of reduction in queen number in the antLasius niger

After the nuptial flight, queens ofLasius nigeroccur in very high densities on the ground. Queens in this study avoided areas frequented by workers of established colonies, leading to additional clumping of nest foundations. In the field 18% of colony foundationnests contained more than one queen (pleometrosis). Queens showed neither preference for nor avoidance of pleometrotic founding, indicating that foundress associations are facultative, promoted by crowding and intense intercolony competition. Indeed, under laboratory conditions brood raiding occurred. In this situation groups of queens had an advantage because they produced more workers initially and the colony with the most workers was more successful in brood raids. The queens in a colony fight until only one is left alive. Removal of workers delayed fighting and addition of workers led to premature fights, indicating that the presence of workers induces fighting amongst the queens. As soon as workers started to forage, additional queens negatively affected colony productivity: colonies with three or four queens produced fewer workers than colonies with one queen. Workers also influenced the outcome of queen-queen interactions, by preferentially feeding the most fertile queen, which was therefore the most likely to survive. Neither weight of the queens by the time of the nuptial flight nor injections of juvenile hormone affected the outcome of fights between queens.

Queen dimorphism and reproductive strategies in the fire ant Solenopsis geminata (Hymenoptera: Formicidae)

Alate trapping studies of a monogyne population of the fire ant Solenopsis geminata indicate that two sizes of gynes are produced. Macrogynes, which participate in late spring and summer mating flights, are larger, fattier, and more than twice as heavy as microgynes, which participate in fall mating flights. Three patterns of gyne production were observed in 51 colonies studied: 35 produced macrogynes only, 9 produced microgynes only, and 7 produced both morphs, contributing to both summer and fall mating flights. Behavioral evidence and rearing studies suggest that macrogynes found new colonies independently, whereas microgynes achieve colony queen status by infiltrating or being adopted by established colonies. Of the total number of female alates collected from the trapped colonies, 56% were microgynes. However, because of their smaller size and lower fat content, microgynes made up only one-third of the caloric investment in female alates. By measuring the thorax lengths of queens from mature colonies, we determined that at least 56% were macrogynes and 35% or more were microgynes. These results indicate that as a reproductive strategy, colony investment in microgyne production may have at least as high a payoff as investment in macrogyne production.

POPULATION STRUCTURE, LOCAL MATE COMPETITION, AND SEX-ALLOCATION PATTERN IN THE ANT MESSOR ACICULATUS.

Population-genetic structure and sex-allocation ratios were investigated for the ant Messor aciculatus, a species that conducts mass nuptial flights. An electrophoretic survey on two polymorphic loci revealed excessive homozygosities in two populations. Because inbreeding inside nests does not occur, the heterozygote deficiency may result from population subdivision rather than assortative inbreeding during nuptial flights. Assuming no inbreeding, a simulation based on the observed genotype distribution in the study site suggested that, on average, a breeding swarm consists of alates from only 1.7 colonies. This population genetic structure seems to cause local mate competition (LMC), a factor that can shift population sex ratio toward females. The sex-allocation ratio to males in the population (0.166 ± 0.030; mean ± SE) was significantly female biased and lower than the expected optima for queens (0.5) and for workers (0.25) without LMC. Sex-ratio variability among colonies was explained by a pattern of constant male investment, which is predictable assuming LMC. Thus, the study provides the first evidence of LMC in ants with mass nuptial flights and contradicts previous assumptions about breeding structure in swarming ants. The results suggest that LMC can affect sex-allocation patterns for ant colonies and populations.

Raiding behavior of the Japanese slave-making antPolyergus samurai

Raiding behavior of the Japanese slave-making antPolyergus samurai was investigated in the field. Raiding trips occurred from early June to early September. A raiding column of several hundreds workers would rush into a target nest and rob mainly worker pupae of the host species,Formica (Serviformica) japonica. Most trips occurred on sunny days. Air temperature, soil temperature, relative humidity, and radiation energy at the ground surface were significantly different between days with and without raiding trips. Nuptial flights occurred on hot, sunny days, and mostPolyergus colonies released alates simultaneously. Behaviors of newly mated queens are also provided and are compared with otherPolyergus species.

The Adaptiveness of Worker Demography in the Attine Ant Trachymyrmex Septentrionalis

Castle theory states that worker size distributions in ant colonies have evolved for efficient division of labor and predicts that they should vary with habitat and have an effect on fitness. We tested these predictions in a comparative study of worker size variation and colony fitness in Florida and Long Island populations of Trachymyrmex septentrionalis. Colonies from the two populations were excavated shortly before the time of the mating flights, so that workers and reproductive forms could be censused. We measured worker head widths in each colony and analyzed the resulting size frequency distributions using the mean, standard deviation, skewness, and kurtoisis, and also principal components derived from these parameters. Size frequency distributions were unimodal and close to normal, with a tendency to negative skewness. Colonies in the Long Island population had both larger workers and greater size variation than those in Florida. Florida colonies followed a growth trajectory in which the mean and standard deviation of worker head width both increased with colony size, whereas in Long Island there was an inverse relationship between the mean and standard deviation that was independent of colony size. Analysis based on the principal components showed that worker size variation significantly affected fitness in both populations, and this was not a secondary effect of colony size. Population differences in colony life history strategies may account for the observed patterns: the Long Island population appears to be adapted for surviving the winter diapause, while the Florida population has experienced different selective pressures, possibly for rapid colony growth. Size variation that has evolved in the context of life history strategies may serve as a preadaptation for division of labor.

Colony level sex allocation in a polygynous and polydomous ant

The colony-level sex allocation pattern of eusocial Hymenoptera has attracted much attention in recent studies of evolutionary biology. We conducted a theoretical and empirical study on this subject using the dolichoderine ant Technomyrmex albipes. This ant is unusual in having a dispersal polymorphism in both males and females. New colonies are founded by an alate female after mating with one or more alate males in the nuptial flight. In mature colonies, the reproductive role of the foundress queen is taken over by wingless offspring (supplementary reproductives). Mature colonies are extremely polygynous, with many wingless queens reproducing through intea-colonial mating with wingless males (inbreeding), and producing both alate and wingless sexuals. The population sex ratio of wingless sexuals was found to be extremely female-biased, while the population allocation ratio of alates was almost 1:1. This result suggests that there is local mate competition among wingless sexuals. A specific model for this extraordinary life cycle predicted that the asymmetry of “regression relatedness” (bf/bm) will disappear during the first few generations of wingless reproductives after the foundress dies. If colonies begin to produce alates after several wingless generations, this undermines the hypotheses for intercolonial sex ratio variation based on the relatedness asymmetry. We compared the magnitude of variation in sex ratios and other characteristics between two levels (within-colony-inter-nest and between-colony). Although there was considerable within-colony variation in all the examined characteristics, between-colony variances were always larger. This means that allocation is important at the whole-colony level, not that of the nest. There was no apparent correlation between the sex ratio of alates and colony size. Furthermore, partial correlation analysis indicated that neither the number of workers nor investment in alates explained the variation in the sex ratio of alates. The only factor which was significantly correlated with the sex ratio of alates was the sex ratio of wingless sexuals (a positive correlation). We conclude that both the alate and wingless sex ratios may be influenced by a common primary sex ratio at the egg stage, the variance of which may have genetic components. In the wingless sexuals, partial correlation analysis indicated that colony size and the number of workers explained the sex allocation ratio. The number of wingless females was strongly (positively) correlated with the total investment in wingless sexuals, while the number of males showed no such correlation. There is, however, no convincing explanation for the variation in sex allocation ratio of wingless sexuals, because the estimates of investment in wingless males may have a large sampling error.