Kazuki Tsuji

Ant reproductive strategies

In contrast to what is generally believed, the reproductive strategies of ants are remarkably diverse and include such different phenomena, as wingless female and male sexuals, reproduction by mated workers, thelytokous parthenogenesis, and complete workerlessness. We review the various reproductive life histories and investigate them in the light of recent models on the evolution of dispersal strategies and multiple-queening. It appears that most deviations from “normal” colony propagation can be explained by a decreased success of dispersal and solitary founding by solitary queens in certain types of habitats. Consequently, alternative reproductive strategies are found especially in those species, in which environmental conditions or a highly specialized way of life are thought to make solitary founding costly. Among the key factors, which determine the success of reproductive strategies, appear to be spatial and temporal distribution of habitats and the availability of nest sites.

Queen and worker policing in the monogynous and monandrous ant, Diacamma sp.

Abstract Policing behavior that prevents workers from laying male eggs was examined in the monogynous and monandrous ponerine ant Diacamma sp. from Japan, in which a singly mated worker called a “gamergate” reproduces as the functional queen in each colony. Since oviposition by virgin workers is rare in the presence of a gamergate, we separated a portion of workers from the gamergates and induced their oviposition experimentally. When orphaned workers had started to oviposit, they were returned to the original colonies, where they continued to lay eggs for a while. The gamergates and other workers interfered with the laying workers by aggressively taking and finally eating the eggs. In total, 60% and 29% of the worker-derived eggs were eaten by gamergates and non-mother workers, respectively. The observed worker-worker interactions were not driven simply by competition to leave own sons, because non-laying non-orphaned workers interfered with worker reproduction. Furthermore, orphaned workers were usually attacked by non-orphaned workers soon after colony reunification. These results indicate that both queen policing by gamergates and worker policing in this species are mechanisms inhibiting worker oviposition. The gamergate contribution to policing was proportionately larger than that of workers, but among virgin workers, the relationship between dominance rank and contribution to policing was not clear. But about 11% of the eggs were not policed and were added to egg piles, especially in large colonies. Worker policing in a monandrous and monogynous eusocial Hymenoptera contrasts to other recent findings, and possible genetic, social, and ecological factors for its evolution in Diacamma sp. are discussed.

Queen Succession Through Asexual Reproduction in Termites

The evolution and maintenance of sexual reproduction may involve important tradeoffs because asexual reproduction can double an individuals contribution to the gene pool but reduces diversity. Moreover, in social insects the maintenance of genetic diversity among workers may be important for colony growth and survival. We identified a previously unknown termite breeding system in which both parthenogenesis and sexual reproduction are conditionally used. Queens produce their replacements asexually but use normal sexual reproduction to produce other colony members. These findings show how eusociality can lead to extraordinary reproductive systems and provide important insights into the advantages and disadvantages of sex.

Secondary polygyny by inbred wingless sexuals in the dolichoderine ant Technomyrmex albipes

SummaryTechnomyrmex albipes makes huge polydomous colonies which consist of up to several millions of adults. In field colonies, dealate queens are rare or absent, though winged males and winged females emerge annually (synchronously) in large numbers from late may to mid June. Field and laboratory observations showed that the reproduction of established colonies was performed by wingless females inseminated by wingless males from the same colony. Dissections and morphological examinations revealed that wingless females are workers with no spermatheca and intercastes with a spermatheca. Most intercastes were inseminated, had developed ovaries, and seemed to reproduce, while workers did not seem to reproduce. Extranidal tasks were performed only by workers. Approximately half of the adult population were intercastes, and wingless males represented only a small portion of all adults, the rest being nonreproductive workers. Intercastes and wingless males were produced throughout the year except in winter. The winged females and males copulate outside the nest only after the nuptial flight and the dealate females are able to perform independent founding, but they are also eventually supplanted by intercastes. The adoption of dealate queens by an established natal colony did not seem to occur. Thus we infer that in this species the winged reproductives disperse and found new colonies, while inbred wingless reproductives allow the enlargement and budding of colonies. This species has a special trophic-flow system. There is no trophallaxis among adults, and nutrient transfer from adults to other colony members is achieved exclusively by specialized trophic eggs. All females (dealate queens, intercastes, and workers) seem to produce trophic eggs. This aphid-like life cycle, i.e., the occurrence of both winged and wingless reproductive forms, may have evolved as an adaptation supporting the development of secondary polygyny and polydomy.

Production of females by parthenogenesis in the ant,Cerapachys biroi

SummaryGroups of virginCerapachys biroi workers produced females (workers) in the laboratories. This is the first report of thelytoky in Cerapachyinae.

Reproductive Conflicts and Levels of Selection in the Ant Pristomyrmex pungens: Contextual Analysis and Partitioning of Covariance

Phenotypic selection on individual- and colony-level characters was examined in the myrmicine ant Pristomyrmex pungens by contextual analysis and partitioning of covariance. Pristomyrmex pungens has an extraordinary social system in which there are no queens and workers reproduce parthenogenetically. All workers can be reproductive and live only one year in this species. Thus, the annual colony growth rate measures the mean individual lifetime reproductive success. Within-colony individual variation in reproductive activity was estimated from individual ovarian development and revealed conflicting selection on worker dimorphism. Large workers are sporadically found in some colonies and had higher fitness on a within-colony level. However, large workers reduced a colonys fitness at the between-colony level. Therefore, large workers probably exist as a socially parasitic phenotype. Stabilizing and positive directional selection on the proportion of foragers appeared to be responsible for the evolutionary maintenance of cooperative breeding in this species. Cheaters that reproduce but never forage will be eliminated by colony-level selection. Overall, directional selection favored smaller colony size. Colony-level adaptation is important, because the mode of colony foundation, fission, is likely to enhance additive genetic variance of colonies and create the opportunity for a genetic response to colony-level selection.

Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators

The Asian weaver ant, Oecophylla smaragdina, is known to have outstanding predatory power. This ant can protect the host plants from attacks of phytophagous insects and therefore has been used for biological control in the tropics. We present evidence for a possible negative effect of Oecophylla on the performance of host plants. Our observation in a fruit orchard of rambutan in Sumatra suggested that the presence of Oecohylla nests on the trees statistically significantly lowered the flower-visiting rate of flying insects, involving the major pollinator Trigona minangkabau. The visiting rate of Oecophylla workers to each flower shoot of rambutan significantly negatively correlated with the visiting rate of flying insects. Empirical evidence of such an inhibitory effect on flower-visiting of pollinators cased by aggressive ants has been scarce so far.

Reproductive conflict among ant workers in Diacamma sp. from Japan: dominance and oviposition in the absence of the gamergate

SummaryQueens do not exist inDiacamma sp. from Japan, and a single worker (“gamergate”) mates and monopolizes reproduction in each colony. We isolated small groups of workers without the gamergate, and confirmed that after 7–15 days many workers were able to oviposit (Tab. 1). These egg-laying individuals engage in stereotyped attacks towards each other. In six groups of individually marked workers (Tabs. 3 to 7), the pattern of aggressive interactions always indicated that one worker was dominant. She usually initiated a large number of attacks, but was herself never attacked. This dominant worker (“alpha”) also ate the eggs just laid by others. There was no linear dominance hierarchy, although a second highest-ranking worker could be recognized (she was only attacked by alpha). When these workers were dissected 4–6 weeks after being orphaned, only the alpha worker had active ovaries; other individuals that had been observed to oviposit earlier exhibited resorbed ovaries. Dissection of another 12 orphaned groups, kept together for different periods of time (Tab. 2), confirmed that one dominant worker is able to suppress the ovarian activity of all others in her group. We discuss how these aggressive interactions also function to regulate the production of males in other contexts, even when the gamergate is present. This aggression is separate, however, from another competitive interaction, mutilation of the gemmae, that functions as a control of mating activity in this species.

Obligate parthenogenesis and reproductive division of labor in the Japanese queenless ant Pristomyrmex pungens

SummaryTwo types of workers were recognized in colonies of Pristomyrmex pungens: extranidal workers (which characteristically walk outside the nest) and intranidal workers (which characteristically stay inside the nest). The ovaries of extranidal workers showed little activity, whereas those of intranidal workers showed high activity and often contained mature oocytes. I therefore conclude that only the intranidal workers reproduce. A behavioral repertoire of 103 individuals was obtained and used to infer group subdivision using cluster analysis; in addition, principal component analysis was performed on the intranidal workers in this set. These data enabled objective separation of extranidal and intranidal workers. Intranidal workers were larger in size on average than extranidal workers; however, the distributions overlapped. Three tests for further subdivision within the group of intranidal workers indicated that such subdivision is weak, and it is also likely that all intranidal workers lay eggs. There was no significant correlation between body size and reproductive status. The number of mature oocytes per ant fitted a Poisson distribution, and the first two principal component factors scores of behavior showed significant correlation with head width. All extranidal workers had resorbed ovaries and also had yellow bodies (which indicated a history of oviposition). When and how the differentiation between the reproductive intranidal workers and the non-reproductive extranidal workers occurred is discussed. The best-supported hypothesis is that extranidal workers are old intranidal ones. Neither males nor inseminated workers were found in any smaples collected in the field or studied in the laboratory, which greatly strengthens earlier suggestions that Pristomyrmex pungens is the first-known ant to be obligately thelytokous. These findings indicate that Pristomyrmex pungens is no longer eusocial, although it has the highest form of social behavior of any thelytokous species; they also raise the question of whether or not there are factors promoting the loss of eusociality and sexuality in this species. Ecological factors are tentatively indicated, namely, the need to maintain large colonies in the face of a nomadic lifestyle involving frequent colony fragmentation.

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.