Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera,Rhinotermitidae)

Summary. Facultative parthenogenesis has great adaptive significance, especially with regard to low pairing efficiency. In the termite Reticulitermes speratus, females that fail to mate with males reproduce parthenogenetically and found colonies cooperatively with partner females or even alone. Comparison of colony foundation success at 400 days between colonies founded by single females (F), female-female pairs (FF), and male-female pairs (FM) showed that female-female cooperation promoted colony survivorship over monogamous foundation. We report here for the first time the mode of parthenogenesis in Isoptera. Combining chromosome observations and genetic analysis using microsatellites, we show that the mode of parthenogenesis is diploid thelytoky and that the restoration of ploidy is most likely accomplished by terminal fusion. Parthenogens show a higher mortality and a longer egg-development time than sexually produced offspring, probably due to reduced heterozygosity. In addition Wolbachia bacteria were detected in R. speratus. However, since Wolbachia was also detected in non-parthenogenetic R. flavipes, it is unlikely that Wolbachia is the cause of parthenogenesis in R. speratus.Received 30 October 2003; revised 4 March 2004; accepted 17 March 2004.     

尖唇散白蚁的孤雌生殖行为及初建群体研究

为了证明尖唇散白蚁Reticulitermes aculabialis Tsai et Hwang是否存在孤雌生殖行为和探讨其初建群体的发育特征,本文对尖唇散白蚁分飞成虫进行雌雌配对（FF）和雌雄配对（FM）人工饲养对比研究。结果显示：FM和FF组的筑巢时间和筑巢活动相似;在建巢初期（配对第5天）FF配对组和FM配对组死亡率分别为11．33％和2．67％,FF配对组死亡率显著高于FM组;产卵前FM组的2只雌性个体和FF组的雌性个体卵巢发育程度一致,都有已经完成卵黄积累的成熟卵母细胞。6个月后,FF配对组有7组产生后代,FM配对组有17组产生后代;FF组子代数目显著低于FM组,分别平均为（7．00±1．58）个和（10．33±1．21）个;FF子代全为2～3龄工蚁,而FM组有由3-4龄工蚁分化的低龄兵蚁。最后,我们对新建群体分化出的第一只兵蚁与成熟巢群中的兵蚁进行了形态学比较。我们的结果表明,尖唇散白蚁具有孤雌生殖行为,并且分飞成虫通过雌雌配对和雌雄配对初建群体在发育模式上有显著差异,雌雌成虫配对采用孤雌生殖方式繁殖有可能是野外尖唇散白蚁建群的另一种方式。     

Preadaptation for parthenogenetic colony foundation in subterranean termites Reticulitermes spp. (Isoptera: Rhinotermitidae)

Thelytokous (all-female producing) parthenogenesis, in some cases, involves reproductive advantages against obligate sexual reproduction. However, the completion of parthenogenesis takes multiple steps without the help of males, and thus preadaptation that meets those requirements will be an important factor for the evolution of parthenogenesis. The Japanese subterranean termite, Reticulitermes speratus, is known to have the ability of parthenogenetic colony foundation, where females that failed to mate with males found colonies cooperatively with partner females and reproduce by parthenogenesis. In this study, we compared the parthenogenetic ability and the colony initiation behavior among six Reticulitermes species in Japan. All species other than R. speratus were not able to reproduce parthenogenetically. Nevertheless, females of these species without the parthenogenetic ability performed homosexual female–female colony initiation and produced eggs without fertilization. In addition, in one species without parthenogenetic reproduction, R. kanmonensis, female–female pair initiated founding behavior as quickly as a heterosexual pair. These results suggest that female–female colony initiation and virgin egg-laying are predominant characters among the genus Reticulitermes and provide a preadaptive condition for parthenogenetic colony foundation in R. speratus.     

Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis

Abstract.  Termite primary reproductives may be exposed to pathogens when dispersing from their parental nest and establishing a new colony. Immunity and reproduction are investigated during colony foundation by implanting a nylon filament into the abdomen of mated and unmated female and male primary reproductives of the dampwood termite Zootermopsis angusticollis. Primary reproductives are paired in combinations of female/male, female/female and male/male and, using confocal microscopy, immune defence is assessed by measuring the degree of encapsulation of nylon implants during three periods of colony foundation: (I) shortly after pairing; (II) during copulation/oocyte maturation; and (III) during oviposition. There are differences in the encapsulation response of mated and unmated termites that are contingent on the period of colony foundation when termites are challenged. Mated females and males have significantly greater encapsulation responses than their unmated counterparts shortly after pairing, perhaps as a prophylactic measure against exposure to disease. The encapsulation response of mated and unmated males does not differ significantly during periods II and III. The onset of oviposition is significantly delayed in mated females that received implants during periods I and II. Mated females have a significantly reduced encapsulation response during the time of copulation and oocyte maturation, but not during oviposition. Overall, males have a significantly greater ability than females to encapsulate a nylon implant. The findings suggest that reproduction can reduce the immune response in female primary reproductives. The results are discussed in light of trade-offs between immunity and reproduction during the critical life-history phase of colony establishment in termites.     

Cooperative colony foundation by termite female pairs: altruism for survivorship in incipient colonies

To determine the costs and benefits of queen association in termites we examined for the first time female-female interactions in colonies founded by two unmated females. In the termite Reticulitermes speratus, females that fail to pair with males found colonies cooperatively with partner females and reproduce by parthenogenesis. We analysed the relationship between queen dominance and initial size ranking in two-queen colonies from the viewpoint of first worker brood production and weight gain. To assign parentage to offspring of two-queen colonies we used mtDNA restriction fragment length polymorphism (RFLP); the results suggested that the two queens produced first worker brood equally throughout colony foundation. Furthermore, initially smaller females gained significantly more weight than initially larger females. This may have resulted from altruistic behaviour of the larger females towards the smaller ones. A simple mathematical model, which considered resource allocation and survivorship, could explain why the larger females behave altruistically towards the smaller females. We also examined the responses of females when more than two females were placed in a petri dish in the presence or absence of a male. If a partner male was present, only one female survived in the colony. In the absence of a partner male, two females, but never more than two, founded a colony cooperatively. These results show that females need a partner to found, and retain, a colony.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Disease and colony establishment in the dampwood termite Zootermopsis angusticollis: survival and fitness consequences of infection in primary reproductives

Pathogens have likely infl uenced life-history evolution in social insects because their nesting ecology and sociality can exacerbate the risk of disease transmission and place demands on the immune system that ultimately can impact colony survival and growth. The costs of the maintenance and induction of immune function may be particularly significant in termites, which have a nitrogen-poor diet. We examined the effect of fungal exposure on survival and reproduction during colony foundation in the dampwood termite Zootermopsis angusticollis by experimentally pairing male and female primary reproductives and exposing them to single (‘acute’) and multiple (‘serial’) dosages of conidia of the fungus Metarhizium anisopliae and recording their survival and fitness over a 560 day period. The number of eggs laid 70 days post-pairing was significantly reduced relative to controls in the serial-exposure but not the acute-exposure treatment. Reproduction thus appeared to be more resilient to a single pathogen exposure than to serial challenge to the immune system. The impact of fungal exposure was transient: all surviving colonies had similar reproductive output after 300 days post-pairing. Our results suggest that disease can have significant survival and fitness costs during the critical phase of colony foundation but that infection at this time may not necessarily impact long-term colony growth. Received 25 February 2005; revised 27 September and 20 October 2005; accepted 20 December 2005.     

The Role of Olfactory Cues in Short-Range Mate Finding by the Emerald Ash Borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae)

We investigated the relative importance of olfaction versus vision in the mate-finding behavior of Agrilus planipennis. When coupled in male–female, male–male and female–female pairs, attempts to mate occurred only in the male–female pairs, suggesting that beetles can identify the opposite sex before attempting to mate. In a set of sensory deprivation experiments with male–female pairs, we evaluated whether males could find females when deprived of their sense of olfaction, vision or both. Males whose antennae were blocked with model paint took significantly longer to find females and spent less time in copula compared to untreated males. Males whose eyes were similarly blocked did not differ in their mate finding capacity compared to untreated males. In a third experiment that compared both olfaction and vision, olfactorily impaired beetles never mated whereas the mate finding potential of visually impaired beetles did not differ from that of untreated beetles. Our results indicate that males can identify females before coming into physical contact with them, and that at short range (≤5 cm), volatile cues detected by olfaction are involved in mate finding by A. planipennis.     

The Mating Behaviour of the Velvet Ant, <Emphasis Type="Italic">Nemka viduata</Emphasis> (Hymenoptera: Mutillidae)

In the present study, the mating behaviour of the velvet ant Nemka viduata (Pallas) (Mutillidae) is described both from field and laboratory observations. The whole pairing interaction, lasting around two hours, includes several behavioural phases. During pre-copula, the male seizes the female’s neck with his mandibles, and then starts to rhythmically stroke the prothorax of the female with his forelegs (this behaviour is also resumed after copulation) before curving his abdomen in order to couple the genital parts, including genital armatures (the male parameres remaining outside the female body); just prior to copulation, the female extrudes the sting, and immediately after copulation begins, she stridulates for 7–10 s, this behaviour is repeated when the pair separates. During copulation (lasting around two minutes), the male moves his antennae rhythmically, hitting the back of the female’s head with the scape. Generally, recently-mated males become aggressive towards females, but more tolerant after a few days. During the whole pairing act, females are held by the males’ mandibles, and in the field they are carried off in flight or by walking to a safe place to copulate. This would suggest that larger males, which can lift a wider range of female sizes, have a reproductive advantage, as indicated by data obtained on their load-lifting capacity with respect to the size distribution of females. A review of mating behaviour in mutillid wasps and comparisons with other lineages of aculeate and non-aculeate Hymenoptera are also given.     

Factors affecting mate choice in the subterranean termite Reticulitermes chinensis (Isoptera: Rhinotermitidae)

Termites are a group of eusocial insects. Mate choice is the most important step which affects the subsequent new colony foundation and development in termites. This study investigated the effects of the four factors on mate choice in the subterranean termite Reticulitermes chinensis Snyder, including colony origin, entry time, physical damage of antennae, and fresh body weights of male dealates. The results showed that the pairing number of dealates from the different colonies was significantly higher than that from the same colonies. The male dealates with early entry time achieved a significantly higher pairing number than the male dealates with late entry time. The male dealates with complete antennae achieved a the significantly higher pairing number than the male dealates lacking the six terminal segments of antennae. Moreover, the heavier male dealates achieved a significantly higher pairing number than the lighter male dealates. However, there were no significant differences in the pairing time for all the experimental treatments. These results suggested that the male dealates, which are heterogenous, healthy, heavy, and more familiar with the environment in R. chinensis, have the obvious advantages in the mate choice. This rule of mate choice is helpful for termites to avoid inbreeding and to maintain the genetic diversity of offspring, which is very important for the environmental adaptability and development of termite colonies.     

Adaptive value of same-sex pairing in Laysan albatross

Same-sex pairing is widespread among animals but is difficult to explain in an evolutionary context because it does not result in reproduction, and thus same-sex behaviour often is viewed as maladaptive. Here, we compare survival, fecundity and transition probabilities of female Laysan albatross in different pair types, and we show how female–female pairing could be an adaptive alternative mating strategy, albeit one that resulted in lower fitness than male–female pairing. Females in same-sex pairs produced 80% fewer chicks, had lower survival and skipped breeding more often than those in male–female pairs. Females in same-sex pairs that raised a chick sometimes acquired a male mate in the following year, but females in failed same-sex pairs never did, suggesting that males exert sexual selection by assessing female quality and relegating low-quality females into same-sex pairs. Sexual selection by males in a monomorphic, non-ornamented species is rare and suggests that reconsideration is needed of the circumstances in which alternative reproductive behaviour evolves. Given the lack of males and obligate biparental care in this species, this research demonstrates how same-sex pairing was better than not breeding and highlights how it could be an adaptive strategy under certain demographic conditions.     

Soldiers are differentiated from male larval stages in incipient colonies of <Emphasis Type="Italic">Nasutitermes takasagoensis</Emphasis> (Isoptera: Termitidae)

In phylogenetically ancestral taxa of termites (the so-called lower termites), at least one soldier emerges and is maintained longitudinally in each incipient colony. However, in apical taxa (the so-called higher termites), the developmental pathway and regulation of soldiers in incipient colonies currently remain unknown. We therefore examined soldier and worker development in incipient colonies of higher termites (Nasutitermes takasagoensis Shiraki). Developmental stages and castes were successfully discriminated by head width in incipient colonies 4 months after colony foundation. Furthermore, differences were observed in the number of bristles on antennae between first- and second-instar larvae. In N. takasagoensis, there was more than one soldier in each incipient colony 4 months after its foundation. Presoldiers in the incipient colonies were differentiated from an earlier instar (male second-instar larvae), whereas, in mature colonies, they were differentiated from male third instars (= minor workers). The developmental period of the former (7 days) was markedly shorter than that of the latter (14 days). All female second-instar larvae molted into workers. The developmental processes shown here are useful for obtaining a clearer understanding of the mechanisms of soldier/worker differentiation in higher termites.     

Asexual queen succession in the subterranean termite Reticulitermes virginicus

Termite colonies are founded by a pair of primary reproductives. In many species, including subterranean termites (family Rhinotermitidae), the primary king and queen can be succeeded by neotenic reproductives that are produced from workers or nymphs within the colony. It is generally believed that these neotenics inbreed within the colony, sometimes for many generations. Here, we show that primary queens of the North American subterranean termite, Reticulitermes virginicus, are replaced by numerous parthenogenetically produced female neotenics. We collected functional female neotenics from five colonies of R. virginicus in North Carolina and Texas, USA. Genetic analysis at eight microsatellite loci showed that 91-100% of the neotenics present within a colony were homozygous at all loci, indicating that they were produced through automictic parthenogenesis with terminal fusion. In contrast, workers, soldiers and alates were almost exclusively sexually produced by mating between the female neotenics and a single king. This is the second termite species shown to undergo asexual queen succession, a system first described in the Japanese species, Reticulitermes speratus. Thus, the conditional use of sexual and asexual reproduction to produce members of different castes may be widespread within Reticulitermes and possibly other subterranean termites.     

Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so‐called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.     

Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata

Summary. In a few, scattered species of social Hymenoptera, unmated workers are capable of producing female offspring from unfertilized eggs through thelytokous parthenogenesis. Regular thelytoky has previously been demonstrated in a number of populations of the neotropical ant Platythyrea punctata. Nevertheless, the finding of males and inseminated queens and workers suggested the sporadic occurrence of sex. In this study we investigated the genetic structure of colonies from Puerto Rico and Costa Rica in order to detect traces of occasional sexual reproduction. Most Puerto Rican colonies had a clonal structure with all nestmates sharing the same multilocus genotype, indicating that thelytoky is the predominant mode of reproduction. Genetic variability was detected in six of 18 colonies and might have arisen from adoption of alien workers in one colony and from the adoption of alien workers, recombination during parthenogenesis, or sexual reproduction in the other colonies. The reproductive of one of these latter colonies was found to be an inseminated worker (gamergate), and the genotypes of its nestmates definitively suggested recombination and sexual reproduction. Three gamergates were found in a single colony collected in Costa Rica, and all produced offspring from fertilized eggs, while uninseminated workers were apparently incapable of reproducing by thelytoky.Received 10 August 2004; revised 20 October 2004; accepted 3 November 2004.     

Bioassay design and length of time in the laboratory affect intercolonial interactions of the Formosan subterranean termite (Isoptera, Rhinotermitidae)

This study examined the effect of diet, experimental design, and length of time in the laboratory on intercolonial agonism among Formosan subterranean termite, Coptotermes formosanus Shiraki, colonies. In pairings of 12 C. formosanus Shiraki colonies collected in an urban forest, there was no significant reduction in survival of termites in 30 out of 59 colony pairs compared to colony controls, but there was <50% survival in 18 colony pairs and <10% survival in six colony pairs. There was no correlation between the level of aggressive behavior and the laboratory diet of the termites. Effect of bioassay design and length of time in the laboratory was evaluated in three colony pairs where tests were first conducted on the day of field collection, then colony pairs were retested every 7 days. Aggressive behavior decreased over time in both bioassays, but it tended to decrease more rapidly in the Petri dish tests. The rapid loss of agonism in groups of termites kept in the laboratory demonstrates that changes in environmental factors affect intercolonial agonism. This article presents the results of research only. Mention of a commercial or proprietary product does not constitute endorsement or recommendation by the USDA.     

Size-assortative pairing in the lotic amphipod <Emphasis Type="Italic">Gammarus zaddachi</Emphasis>, an examination of hypotheses and the influence of current speed

Three main hypotheses have been put forward to explain size-assortative pairing in gammarid amphipods: microhabitat separation, sexual selection and loading constraint. In order to determine which hypothesis best explains this phenomenon in the estuarine species Gammarus zaddachi, I first measured the body lengths and dry weights of precopula pairs collected from two field sites with substantially different current speeds. Second, I performed three laboratory experiments in order to estimate the importance of the following processes: (1) male choice; (2) male–male competition and (3) male–female acceptability. The loading constraint hypothesis seemed best supported by the data in that field-collected male G. zaddachi size correlated well with female size in precopula pairing in both fast and slow flowing water. In the laboratory, males preferred females of their same size group (large versus small), and ‘won’ them in the male–male competition experiments. Size-assortative pairing is thus likely a consequence of the loading constraints imposed upon these males by virtue of them having to carry and manoeuvre their partners through flowing water, while attempting to maintain station in an optimal microhabitat. Males may therefore forego the largest, most fecund females, in favour of a practicable payload (small male–large female pairings were rare). However, there seems to be a lower limit to this selection, indicated by the high degree of cannibalism on small females by large males.     

Female ornamentation, parental quality, and competitive ability in the rock sparrow

The evolution of female ornaments is poorly understood. Recent evidence suggests not only that female ornaments may be genetic correlates of selection on males but may also have evolved through male mate choice and/or through female–female aggressive interactions. In the rock sparrow, Petronia petronia, both sexes have a carotenoid-based yellow patch that is sexually selected by both sexes. The benefits that male may gain from choosing an attractive female remain unidentified. Both parents participate in caring for the young, so there should be mutual mate choice because males and females should both benefit from choosing a good parent (good parent hypothesis; GPH). Moreover, it has already been demonstrated that the yellow patch in males is also a badge of status (armament). Therefore, the yellow patch could also serve as both ornament and armament in females (dual utility hypothesis; DUH). We investigated the hypothesis that male and female yellow patch size signals parental quality in the field. We tested by an experiment in captivity the signal function of the yellow patch in female–female aggressive interactions for access to food. Yellow patch size correlated with paternal, but not maternal, feeding rates. Thus, this study supports the hypothesis that yellow patch dimension signals male parental quality, but there is no evidence for the GPH to explain female ornamentation. In the experiment females with relatively large yellow patches had earlier access to food than those with small patches. These results seem to suggest that a sexually selected carotenoid-feather signal may be used in female–female competition, in agreement with the DUH. Males may benefit from choosing well ornamented females because these may be superior competitors.     

Biparental care in incipient colonies of the dampwood termiteZootermopsis angusticollis Hagen (Isoptera: Termopsidae)

Parental care and division of labor in male and female primary reproductives in incipient colonies of the dampwood termite Zootermopsis angusticolliswere studied by recording repertory sizes, behavior frequencies, time budgets, and transition probabilities of acts. Repertory sizes for males and females were identical, and behaviors were performed at similar frequencies. Time budget data also suggested equal participation in parental care by both sexes. Transition probability analysis suggested that males and females did not organize their behavior in roles. We therefore found no indication of sex-based division of labor during colony foundation and the incipient stages of colony growth. The lack of behavioral specialization may be due to the fact that acts might be related and/or have more than one function, and different tasks are not spatially associated. Our observations are consistent with the hypothesis that monogamous mating systems in termites involve mate assistance.     

Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula

Abstract.— We investigated sex allocation in a Mediterranean population of the facultatively polygynous (multiple queen per colony) ant Pheidole pallidula . This species shows a strong split sex ratio, with most colonies producing almost exclusively a single-sex brood. Our genetic (microsatellite) analyses reveal that P. pallidula has an unusual breeding system, with colonies being headed by a single or a few unrelated queens. As expected in such a breeding system, our results show no variation in relatedness asymmetry between monogynous (single queen per colony) and polygynous colonies. Nevertheless, sex allocation was tightly associated with the breeding structure, with monogynous colonies producing a male-biased brood and polygynous colonies almost only females. In addition, sex allocation was closely correlated with colony total sexual productivity. Overall, our data show that when colonies become more productive (and presumably larger) they shift from monogyny to polygyny and from male production to female production, a pattern that has never been reported in social insects.     

Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera,Kalotermitidae)

The existence of altruism in social insects is commonly attributed to altruistic individuals gaining indirect fitness through kin selection. However, recent studies suggest that such individuals might also gain direct fitness through reproduction. Experimental studies on primitive wood-dwelling termites revealed that colony fusion often causes the death of primary reproductives (queen and king), allowing opportunities for workers to inherit the nest by developing into replacement reproductives (neotenics). Therefore, colony fusion has been proposed as an important factor that may have favoured sociality in termites. However, whether colony fusion occurs frequently in natural populations of wood-dwelling termites remains an open question. We analysed eleven colonies of the wood-dwelling termite Kalotermes flavicollis (Kalotermitidae), using two mitochondrial and five nuclear microsatellite markers. Nine of eleven colonies (82%) were mixed families, with offspring of three or more primary reproductives. To our knowledge, this result represents the highest frequency of mixed-family colonies ever reported in termites. Moreover, genetic mixing of colonies appeared extreme in two ways. First, the number of haplotypes per colony was exceptionally high (up to nine), indicating that colonies were composed of multiple queens' offspring. Second, some mixed-family colonies included individuals belonging to two highly divergent genetic lineages. F-statistics and relatedness values suggest that mixed-family colonies most likely result from colony fusion, giving support to the accelerated nest inheritance theory. These findings raise important questions about the mode of foundation of mixed-family colonies and the evolutionary forces that maintain them within populations.