Long-term impact of orphaning on field colonies ofCoptotermes lacteus (Froggatt) (Isoptera: Rhinotermitidae)

Summary Colonies ofCoptotermes lacteus (Froggatt) from a site in coastal south-eastern Australia were experimentally orphaned in early 1989. Sample colonies were examined 3, 6, 12, 18, 24 or 30 months later for their caste composition, the presence of replacement reproductives and brood. All replacement reproductives were nymphoid neotenics. The number of functional (physogastric) females ranged from 1 to 27; this variability was maintained irrespective of the length of time between orphaning and inspection of the colonies. The average live mass of individual females stayed at 30 to 40 mg over the period of 6 to 30 months after orphaning in groups of more than five neotenic queens, but increased from 38 mg three months after orphaning to about 125 mg after 24 months in colonies headed by fewer than five neotenic females. The combined live mass of neotenic females could approach or even exceed that of primary queens. Two key features characterized experimentally and naturally orphaned, neotenic-headed colonies: (1) Nymphs differentiated in significant numbers all year round for a period of at least 30 months right from the time neotenics commenced breeding (in primary-headed colonies nymph production is strictly seasonal). (2) All or most nymphs were males (in primary-headed colonies the sex ratio of nymphs is more or less balanced). The mechanism(s) for achieving the male-biased sex ratio is (are) unknown. Even when colonies have resumed breeding with the help of neotenics, colony survival is not guaranteed. Under such circumstances the gene pool is best preserved if colonies were to raise and release large numbers of alates as potential founders of new colonies. By producing largely male nymphs orphaned colonies ensure outbreeding and may prevent competition (and its disruptive impact an breeding) between existing reproducing neotenic queens and newly differentiating female neotenics. Competition between male neotenics is unlikely to have any impact on the rate of brood production and therefore would not require a mechanism to prevent it from occurring.     

Benefits and costs of secondary polygyny in the dampwood termite Zootermopsis angusticollis

Newly molted female neotenic reproductives of the dampwood termite Zootermopsis angusticollis Hagen were allowed to mature in the presence of a neotenic male, a fixed number of larval helpers, and varying numbers of sibling neotenic queens to assess the impact of secondary polygyny to the individual and colony. Under monogyne conditions, neotenics developed more ovarioles per ovary and had higher individual fecundities after 60 d compared with females under polygyne conditions. Queens in groups of three females were able to gain more body mass than those in groups of five. Although the division of resources provided by helpers reduced individual female development and fecundity under polygyne conditions, it resulted in an overall increase in colony fecundity. In addition, neotenic females in polygynous colonies did not differ significantly in reproductive competence. There was no evidence that neotenics were attacked or injured by other reproductives or larval helpers, suggesting little if any reproductive competition among sibling queens. The physiological responses of neotenics to the increasing queen/worker ratio may have the benefit of enhancing the colony growth at the cost of the fecundity of individual queens.     

Patterns of neotenic differentiation in a subterranean termite, Reticulitermes speratus (Isoptera: Rhinotermitidae)

Plasticity in the caste developmental pathway is a remarkable characteristic of termite societies. In Reticulitermes, two types of neotenic reproductive, nymphoids and ergatoids, may differentiate from nymphs and workers and take over reproduction in the colony after the death of the original primary reproductive pair. We examined the dynamics of newly differentiated nymphoids and ergatoids in experimentally orphaned laboratory colonies of R. speratus with different caste compositions. The period required for differentiation of nymphoids was shorter than that for differentiation of ergatoids. The sex ratio of neotenics was strongly female‐biased, particularly in ergatoids. The results suggested that the number of differentiated ergatoids was restricted by the existence of nymphs or nymphoids in a colony. Workers were assumed to kill most newly differentiated neotenics. Attack reflecting conflict between colony members is probably an important mechanism to control neotenic emergence.     

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.     

Response to orphaning in two Neotropical termites: shape Armitermes euamignathus and shape Embiratermes festivellus

In this paper we examine the potential of the termites Armitermes euamignathus Silvestri: 1901 and Embiratermes festivellus (Silvestri, 1901) (Isoptera, Termitidae, Nasutitermitinae) to produce neotenics experimentally. Three nests of the mound-building termite A. euamignathus, from the Brazilian cerrado, had their primary queens removed in August 1994. After 12 months, only one mound survived; it had a normal appearance. In this healthy, orphaned colony we found the primary king, six physogastric nymphoid female replacement reproductives, two ergatoid female replacement reproductives, 46 nymphs, several presoldiers, soldiers, workers, larvae and many eggs. These data show that neotenics in A. euamignathus may originate from both workers and nymphs, but nymphoids are produced in larger numbers. The biometric study of nymphs and nymphoids suggests that these brachypterous neotenics were derived from third instar nymphs after a single moult or from four instar nymphs after a reduction of wing bud length. A piece of an E. festivellus nest with some third instar nymphs, soldiers and workers was kept under laboratory conditions. After 12 months, the whole experimental subcolony was examined and appeared to contain two pigmented nymphoid females, two pigmented nymphoid males, only one larva, seven nymphs of the same instar, 148 workers, five soldiers and many eggs. These results also indicate the capacity of the termite E. festivellus to produce nymphoid neotenics. These neotenic females were laying eggs, but they were not physogastric after a year, unlike some nymphoids of the same species collected from natural colonies.     

The influence of group size on ovarian development in adult and neotenic reproductives of the termite Zootermopsis angusticollis (Hagen) (Hodotermitidae)

Termite imagines of Zootermopsis angusticollis (Hagen), while still in the colony as winged individuals, do not show ovary development, although vitellogenin is present in the blood at low levels. When removed from the colony, artificially dealated, and paired, vitellogenin levels rise: subsequently ovaries develop resulting in oviposition approximately 15–16 days after removal from the colony. Imagines removed from the colony, dealated and held together in a heterosexual group, however, show little or no ovary development after 25 days, although vitellogenin is present in the haemolymph in low levels. Newly developed neotenic reproductives, on the other hand, removed from the colonly 1–2 days after the neotenic moult, and isolated in heterosexual pairs for 60 days, had ovaries which did not become larger than 0.02 mm³, and no eggs were laid. This is in contrast to the normal ovary development of neotenic reproductives produced in groups of larvae, as described earlier. Vitellogenin levels in isolated pairs of neotenics were low until 25 days after isolation, while vitellogenin levels increased 7–9 days after the moult in female neotenics kept in a colony with larvae. The results of this study on ovarian development and vitellogenesis in neotenic and adult reproductives reflect the normal biology of the two reproductive types where the latter leave the colony to found new colonies, while neotenics become sexually mature within the colony in which they developed.     

Ontogenic potentialities of the worker caste in two sympatric subterranean termites in France

In termites, the capacity of workers to differentiate into neotenic reproductives is an important characteristic that deserves particular attention. To gain insight into the differentiation pathway, the potentialities of workers and the endocrinal changes during the formation of neotenics were compared in two sympatric termites, Reticulitermes flavipes and Reticulitermes grassei. After 1 year of development, 100% of R. flavipes worker groups produced neotenics against only 63% of R. grassei groups. The average production of female neotenics was significantly higher in R. flavipes worker groups compared with R. grassei groups and R. flavipes produced a greater proportion of female neotenics. Moreover, R. flavipes produced more offspring, not only because there were more females, but also because R. flavipes females were more productive. Moreover, the offspring produced by R. flavipes grew faster than the offspring of R. grassei. Both ecdysteroid and juvenile hormone (JH) titers varied significantly during the development of neotenics. The two species showed similar ecdysteroid titer variation patterns. However, the JH titer variation patterns strongly differed: in R. grassei, the concentration of JH increased in maturing neotenics then dropped in mature neotenics, whereas in R. flavipes, the level of JH was significantly higher than in R. grassei and remained constantly high in mature neotenics. Overall, these results suggest that these two species differ strongly in many life-history traits as well as in the physiological control of their caste differentiation system. Possible origins and mechanisms of such interspecific variations are discussed, as well as their evolutionary and ecological consequences.     

圆唇散白蚁雌性补充生殖蚁不同发育阶段表皮长链碳氢化合物的变化

【目的】确定圆唇散白蚁 Reticulitermes labralis 补充生殖蚁不同发育阶段表皮长链碳氢化合物(cuticular long-chained hydrocarbons, CHCs) 的变化。【方法】人工隔离巢群饲养圆唇散白蚁 R. labralis,观测其翅芽型补充生殖蚁的分化时间和补充生殖蚁数量趋于稳定的时间,并采用气质联用仪(GC-MS)对补充生殖蚁不同发育阶段的表皮长链碳氢化合物变化趋势进行分析。【结果】随着补充生殖蚁的出现,每一巢群会逐渐形成稳定数量的具有生殖能力的生殖蚁。若蚁在分化为补充生殖蚁的第8天时,43.3%的组补充生殖蚁数量趋于稳定,第16天时83.3%的组趋于稳定,第25天时93.3%的组趋于稳定,36 d后100%的组趋于稳定。通过补充生殖蚁不同发育阶段中CHCs各峰面积与若蚁阶段相应峰峰面积的比值随发育阶段的变化趋势分析发现,在卵中没有检测到的保留时间为38.52 min的化合物在补充生殖蚁产7~8粒卵时峰面积比值是若蚁阶段的14.14倍;在卵中检测到的保留时间为35.50和39.21 min的峰面积比值在补充生殖蚁开始产卵后显著升高。【结论】CHCs不能用来区分有无生殖能力的补充生殖蚁个体,但可以很好地用来区分补充生殖蚁个体与尚未转化为生殖蚁的若蚁个体;保留时间为38.52 min的化合物是补充生殖蚁的特有物质;保留时间为35.50和39.21 min的化合物可作为补充生殖蚁已经产卵的标志。     

Changes in juvenile hormone synthesis in the termite Reticulitermes flavipes during development of soldiers and neotenic reproductives from groups of isolated workers

Workers of Reticulitermes flavipes were isolated in groups of increasing numbers to determine the in vitro rates of juvenile hormone (JH) synthesis by individual pairs of corpora allata (CA) as other castes differentiated. Only neotenic reproductives developed in groups of 12. Mean JH synthesis rates increased after 5 weeks but only a few individuals had significantly higher rates, about 0.4 pmol/pair/h, which occurred at about 3 weeks before neotenics developed. Soldiers and neotenics developed in groups of 50. Mean rates increased to a peak at week 6 after isolation, but only a few individuals had rates approaching 1 pmol/pair/h, which occurred at the same time after isolation as the development of pre-soldiers. JH synthesis by CA of pharate pre-soldiers and soldiers was low compared to that of pharate workers and neotenics. CA of pre-soldiers attained a peak mean rate of JH synthesis of 0.9 pmol/pair/h at 6 days of age, whereas CA of soldiers attained only a peak mean rate of 0.3 pmol/pair/h. These measurements of JH synthesis by individual pairs of CA suggest that the few workers destined to become pre-soldiers have 2.5-fold higher JH synthesis than the few that would develop into neotenic reproductives, and show that a cycle of synthesis accompanies the development of pre-soldiers into soldiers.     

Workers do not mediate the inhibitory power of queens in a termite, <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera,Rhinotermitidae)

In social insects, the caste systems are based on reproductive division of labor; queens specialize in reproduction and workers primarily maintain the colony. Recently, a volatile pheromone containing n-butyl-n-butyrate and 2-methyl-1-butanol was identified as a termite queen pheromone that inhibits the differentiation of female neotenic reproductives (secondary queens). Although this volatile inhibitory pheromone regulates caste differentiation directly, the method by which it reaches members without direct contact with the queen in large colonies is not well understood. Therefore, additional mechanisms of indirect communication must exist, such as worker-mediated queen signal transport. We found that workers exposed to female reproductives did not mediate queens’ inhibitory signal in a termite Reticulitermes speratus. The experiment assessed worker transfer from direct to indirect contact groups and determined that the differentiation of new female reproductives in the indirect contact groups was not influenced by the direct contact groups, whereas direct contact with functional female reproductives and artificial queen pheromone did suppress neotenic differentiation. This suggests that worker transfer of the queen signal is unlikely and that for colony-wide inhibition direct contact by the majority of infertile members with reproductives or eggs, which emit the same volatiles as female reproductives, is necessary within a certain time interval.     

Parthenogenetic reproduction in neotenics of the subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae)

Experiments with artificial colonies consisting of only female workers and those of female nymphs and workers of a subterranean termite, Reticulitermes speratus, showed that neotenics (ergatoids and nymphoids) can reproduce parthenogenetically. The larvae hatched from the eggs produced partheno‐genetically by the neotenics were all female and did not have any aberrant external morphology. They had 42 chromosomes and were diploid. The analysis of genotypes at microsatellite loci revealed that the eggs produced parthenogenetically had only one of the two alleles that the mother neotenics possessed, indicating that the eggs were produced by automixis.     

Value of male remating and functional sterility in redback spiders

In the Australian redback spider, Latrodectus hasselti, males typically use their paired copulatory organs (palps) to copulate twice with a single female then sacrifice themselves to their cannibalistic mates in a strategy that increases their paternity in that one mating, but leads to death. This type of terminal investment in one mating is predicted only if the expected value of future matings is low for males relative to the value of repeated mating with the same female. In this laboratory study, we quantified the reproductive value of mating more than once with the same female (repeated mating) and mating with more than one female (multiple mating) for male redback spiders. We tested two natural selection hypotheses for repeated mating, sperm limitation and reproductive insurance, but found no support for either hypothesis. We show that, in the absence of sperm competition or cannibalism, male lifetime reproductive output is the same whether a male copulates once, twice, or several times with a given female. Repeated mating does not increase the probability of successful fertilization, nor does it increase the number of offspring produced in successful matings. Although male repeated mating is not favoured because of increased fertility of mates, other studies suggest it may be important in sperm competition. Here we show that the relative reproductive value of the first two copulations is very high for redback males because they are functionally sterile after each palp has been used once; nonvirgin males are unable to father offspring. Functional sterility and repeated mating by male redbacks may be favoured by the same factors that lead to male sacrifice behaviour: ecological constraints on multiple mating combined with competitive benefits of maximal investment in the first mating. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sex ratio determination by queens and workers in the ant Pheidole desertorum

Because workers in colonies of eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts workers should bias investment in reproductive broods to favour reproductive females over males. However, conflict between queens and workers is predicted. Queens are equally related to daughters and sons, and should act to prevent workers from biasing investment. Previous study of the ant Pheidole desertorum showed that workers are nearly three times more closely related to reproductive females than males; however, the investment sex ratio is very near equal, consistent with substantial queen control of workers. Near-equal investment is produced by an equal frequency of colonies whose reproductive broods consist of only females (female specialists) and colonies whose reproductive broods consist of only males or whose sex ratios are extremely male biased (male specialists). Because natural selection should act on P. desertorum workers to bias investment in favour of reproductive females, why do workers in male-specialist colonies rear only (or mostly) males? We tested the hypothesis that queens prevent workers from rearing reproductive females by experimentally providing workers with immature reproductive broods of both sexes. Workers reared available reproductive females, while failing to rear available males. Worker preference for rearing reproductive females is consistent with queens preventing their occurrence in colonies of male specialists. These results provide evidence that queens and workers will act in opposition to determine the sex ratio, a fundamental prediction of queen-worker conflict theory. Copyright 2000 The Association for the Study of Animal Behaviour.     

COLONY SEX RATIOS,CONFLICT BETWEEN QUEENS AND WORKERS,AND APPARENT QUEEN CONTROL IN THE ANT PHEIDOLE DESERTORUM

Sex-ratio conflict between queens and workers was explored in a study of colony sex ratios, relatedness, and population investment in the ant Pheidole desertorum. Colony reproductive broods consist of only females, only males, or have a sex ratio that is extremely male biased. Colonies producing females (female specialists) and colonies producing males (male specialists) occur at near equal frequency in the population. Most colonies apparently specialize in producing one reproductive sex throughout their life. Allozyme analyses show that relatedness does not differ within male-specialist and female-specialist colonies and they do not appear to differ in available resources. In the population, workers are nearly three times more closely related to females than males; however, the investment sex ratio is near equal (1.01, female/male), which is consistent with queen control. Selection should be strong on workers to increase investment in reproductive females, so why do workers in male-specialist colonies produce only (or nearly only) males? One hypothesis is that queens in male-specialist colonies prevent the occurrence of reproductive females, perhaps by producing worker-biased female eggs. An earlier simulation study of genetic evolution of sex ratios in social Hymenoptera (Pamilo 1982b) predicts that such mechanisms can result in the evolution of bimodal colony sex ratios and queen control. Results on P. desertorum are generally consistent with that study; however, information is not currently available to test some of the model's predictions and assumptions.     

Is Fatter Sexier? Reproductive Strategies of Male Squirrel Monkeys (Saimiri sciureus)

Sexually dimorphic traits can evolve through male–male competition or female choice. Squirrel monkeys (genus Saimiri) live in large multimale, multifemale groups and are seasonal breeders with concealed ovulation. In several species of the genus, females are dominant to males. Males show weight gain preceding and during the mating season, which produces a “fattened” appearance in the upper arms, shoulders, and torso. Although much is known about the physiology of fattening, the evolutionary function(s) of this sexually dimorphic trait, including possible benefits and costs, remain(s) unknown. This unusual reproductive physiology of males is suggestive of sexual selection. Here I present data on wild Saimiri sciureus studied in Brazil to describe male reproductive investment in the species and to examine the hypothesis that male fattening is a product of sexual selection. I observed at least nine adult males via focal animal sampling and ad libitum observations during four mating seasons and during an additional 10 nonbreeding season months for comparison. Compared to less robust males, fatter males spent significantly more time near females and less time alone. These males also spent more time engaged in sociosexual activities and less time feeding/foraging, suggesting a trade-off between maintenance and reproductive behaviors. The 2-mo mating season accounted for 62% of all male–male agonism observed over one 12-mo period. These results are suggestive of male–male competition for females. However, males did not coerce females to mate and females often rejected males; this pattern suggests female choice. It is possible that male fattening in Saimiri is a product of both intra- and intersexual selection. Males experience intense reproductive costs related to agonism with other males, and related to time and energy invested in the pursuit of females. Although fattening may mitigate some of these costs by aiding in male–male competition and in female preference, this phenomenon is likely not without physiological costs to adult males.     

Evidence of extreme habitat stability in a Southeast Asian biodiversity hotspot based on the evolutionary analysis of neotenic net-winged beetles

The diversification of neotenic beetle lineages has not been studied, despite the potential for defining biodiversity hotspots and elucidating the history of regional faunas. Additionally, neotenics may provide insight into the process of speciation in small populations with extremely low dispersal ability and a limited range. Here, we used two rDNA and three mtDNA markers to investigate the phylogeny of Scarelus, a neotenic lineage endemic to Southeast Asian rainforests. Most genetic differentiation was associated with Palaeogene geographical divisions, which remain distinct despite temporary connections. Dispersal events were rare, with only two inferred for Scarelus: from Borneo to the Philippines 28.3 million years ago (Ma) and from Sumatra to Java 13.9 Ma. We suggest that speciation resulted from allopatric range fragmentation, and Scarelus diversified readily when conditions were favourable; in this case, at different times in the eastern (19.3-39.1 Ma) and western (3.5-13.9 Ma) parts of Sundaland. The observed strong phenotypic similarity was preserved under speciation through complete allopatry. Neotenic Lycidae have survived for a long time in very stable habitats, and extremely low dispersal activity has not limited their persistence; however, the long-term diversification rate of neotenics is low and diversification is nonexistent under stable conditions. The modern ranges of neotenic lineages are indicative of ancient rainforest refugia and may be used in biodiversity conservation management. Most neotenics are at risk of extinction because of their small ranges and a low dispersal potential.     

Termite colony ontogeny: a long-term assessment of reproductive lifespan, caste ratios and colony size in Reticulitermes flavipes (Isoptera: Rhinotermitidae)

Thirty Reticulitermes flavipes (Kollar) colonies established by alates collected from two separate field sites were raised in the laboratory for eight years. Twenty-one of the colonies were founded by alates from one field source and nine from another, providing demographic data from two unrelated parental lineages. Colony totals ranged from 3620 to 11641 individuals, with no significant difference in size between lineages. Soldier caste proportion of the colony total and mean wet weights for workers, soldiers and kings were significantly different between the two lineages. This suggests that at least a portion of the variability observed in caste ratios and body size may be heritable. One founding reproductive had died in five of the colonies (17%); none lost both parents. The queenless colonies contained exclusively female replacement reproductives (neotenics); the kingless colony contained a female-skewed mixture of male and female neotenics. All the nests that lost a founding parent contained significantly more pre-alate nymphs than the nests with both a king and a queen. Comparisons with published reports of ontogenetic patterns in other termites and social insects are discussed.     

Caste-biased locomotor activities in isolated termites

Eusocial insects are characterized by a well-developed division of labour among castes. Although the successful division of labour should stem from behavioural differentiation depending on caste identity, caste-specific intrinsic behavioural characteristics might be masked by social interactions within colonies. The present study explores caste-specific intrinsic locomotive activities of termites by quantifying them in isolation. We track individual movement trajectories of the damp-wood termite Hodotermopsis sjostedti over 30 min and extract individual locomotion parameters. Multivariate statistical analyses reveal significant differences among castes: soldiers move more actively than workers and neotenic reproductives. The morphometric data of test individuals indicate that locomotor activities reflected caste identity more strongly compared with quantitative morphological variations among individuals. We find that the different locomotor activities of soldiers compared with those of neotenics and workers probably reflect their physiological differentiation. The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.