A novel hypothesis for the origin of the sexual division of labor in termites: which sex should be soldiers?

Sexual specialization and skewed sex ratios of the altruistic castes, especially soldiers, are common in many termite taxa. However, no theoretical or empirical studies have explained the origin of the sexual division of labor in termites. In most termite species, female alates are larger than male alates, and mature queens are much larger than kings, with females under consistent selection for high fertility. Therefore, females usually have the potential to be larger than males. Here, I present a novel preadaptation hypothesis that potential sexual differences in the suitability for the caste give rise to the sexual division of labor, and I provide the first evidence in support of this hypothesis in termites. Defense in Reticulitermes is typically performed by soldiers via mandibular and phragmotic defense in which soldiers with pluglike heads block openings, thus preventing enemies from invading the nest. Phragmotic defense requires that soldiers have heads wide enough to plug nest openings. Therefore, a size threshold for workers that develop into soldiers is a likely adaptation for effective defense. I show that sexual size dimorphism (SSD) and a size threshold for soldiers promote skewed sex ratios. A female-biased soldier sex ratio was observed in species with SSD, whereas there was no bias in soldier sex ratio in species without SSD. Thus, SSD and soldier sex ratio data from several Reticulitermes species support the preadaptation hypothesis.     

两种鼻白蚁之间的入侵关系

设计了5个实验以研究台湾乳白蚁(Coptotermes formosanus)和黄肢散白蚁(Reticulitermes flavipes)的种间斗争关系。所试白蚁来自阿拉巴马州。实验1将两组白蚁的兵蚁和工蚁以自然比例混合(台湾乳白蚁工蚁：兵蚁＝20：5,黄肢散白蚁工蚁：兵蚁＝24：1);实验2观察了双方同数量(各25头)工蚁的种间斗争能力;实验3观察两者同数量(各5头)兵蚁的种间斗争关系;实验4、5分别研究双方工蚁与兵蚁的斗争关系。因两种工蚁形态相似,所以在实验前用0．1％Nile blue A染过的滤纸饲喂一方白蚁24h使虫体着色以便观察。所有实验在22℃,65％RH荧光灯下进行。每个实验将两方白蚁同时放入一培养皿中,观察至一方100％受伤,然后把培养皿移到培养箱内,24小时后统计死亡率。结果表明,实验一开始,双方的工蚁和兵蚁都立即进入残酷的厮杀斗争,台湾乳白蚁兵蚁和工蚁的斗争能力都明显强于黄肢散白蚁;兵蚁的斗争行为不受工蚁的影响,工蚁的斗争能力也不受兵蚁的制约。实验中台湾乳白蚁的工蚁与黄肢散白蚁的兵蚁攻击能力相当,但黄肢散白蚁的工蚁却远弱于台湾乳白蚁的兵蚁。上述结果说明,自然界中不可能出现此两种白蚁群体的偶然性融合;外来的台湾乳白蚁很可能在其群体建立的地区占据优势[动物学报49(3)：295—302,2003]。     

Cuticular permeability of two species of Coptotermes Wasmann (Isoptera: Rhinotermitidae)

Cuticular permeability (CP) values of worker and soldier castes of Coptotermes formosanus Shiraki and Coptotermes vastator Light were determined using gravimetric techniques. Comparisons were made between castes, species, and between colonies of C. formosanus and C. vastator. CP values did not differ among either species or colony, however they did differ between castes. Data reported here and that of established data in the literature for C. formosanus are inconsistent, with the current report having values as small as half that of previously published data. Examining mean CP data by colony indicated that there is a range for Coptotermes spp. termites, from 6.84+/-1.2 to 25.61+/-1.49 microg H(2)Ocm(-2)mmHg(-1)h(-1) dependent upon caste. A novel method of examining intercaste CP variability is the use of worker:soldier CP ratios. Ratios for C. formosanus were consistent between the current study and previous reports. Mean percentage total body water (%TBW) lost at the time of death was 33.75+/-1.15% (soldiers) and 54.24+/-1.43% (workers) for C. formosanus, and 37.69+/-3.31% (soldiers) and 52.87+/-3.65% (workers) for C. vastator. Consistently, %TBW (and fresh mass) was greater in worker than in soldier castes. These data suggest the use of water storage mechanisms in worker termites, as shown for other rhinotermitids.     

Fire ant predation on native and introduced subterranean termites in the laboratory: effect of high soldier number in Coptotermes formosanus

Abstract.

• 1 Native Reticulitermes spp. Holmgren and the introduced Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) were exposed to predation in the laboratory by Solenopsis invicta Buren (Hymenoptera: Formicidae), a known predator of Reticulitermes.
• 2 In one experiment, both taxa contained the 2.4% soldiers commonly found in Reticulitermes. In a second experiment, Reticulitermes contained 2.4% and C.formosanus a more normal 18.3% soldiers.
• 3 When soldier proportions were equal, C.formosanus soldiers suffered less of a decrease in survivorship due to predation compared with Reticulitermes soldiers. Little difference was found between taxa in the effect of predation on termite workers or in the effect of termites on predator survivorship.
• 4 When soldier proportions were unequal, both C.formosanus castes suffered less from predation than those of Reticulitermes. Again, little difference was found in the effect of termites on ants.
• 5 C.formosanus showed less movement into new containers when soldier number was abnormally low, compared with both taxa with normal caste proportions.

     

Differences in cellulose digestive systems among castes in two termite lineages

Abstract.  Termites (Isoptera) are eusocial insects and express polyphenism. Soldiers have specialized morphology for colony defense, but their feeding activity is dependent on other colony members. To determine differences in cellulose degradation between soldier and worker termites, enzymatic activity and cellulase gene expression, as well digestive tract histology, are examined in two phylogenetically distant species. In Hodotermopsis sjostesti (family Termopsidae) , endo-β-1,4-glucanase activity is identified in the salivary glands, whereas β-glucosidase activity is identified in salivary glands and hindgut. The relative expression levels of endo-β-1,4-glucanase genes in soldiers are significantly lower than in workers. Thin sections of salivary gland of workers and soldiers are different in H. sjostedti . In Nasutitermes takasagoensis (family Termitidae), the endo-β-1,4-glucanase activity is restricted to the midgut in four tested castes (i.e. three types of workers and soldier). Examination of activity per termite reveals the highest activity in minor workers and the lowest activity in major workers and soldiers. The β-glucosidase activity is also concentrated on the midgut in all four castes. The relative expression level of the endo-β-1,4-glucanase gene does not correspond with its activity in the midgut. In thin sections prepared from N. takasagoensis , the folds and pulvillus in the gizzards, and cuticle structure of soldiers are less developed compared with the other three worker castes. The differences in digestive system among termite castes in terms of caste development in each species are discussed.     

Colony demographics of rare soldier-polymorphic worker caste systems in <Emphasis Type="Italic">Pheidole</Emphasis> ants (Hymenoptera,Formicidae)

Nearly all species in the ant genus Pheidole have dimorphic workers, with distinct small minors and larger soldiers. The size range of both castes is typically narrow. Just seven described species are soldier-polymorphic, with a broad soldier size range. Here, we characterize worker caste allocation and demography in the soldier-polymorphic P. obtusospinosa, P. rhea, and P. tepicana, and the dimorphic P. spadonia for comparison. The head allometry of soldiers in soldier-polymorphic species is strongly positive and that of dimorphic species is negative. Among soldier-polymorphic species, the soldier castes differ from each other in the degree of positive allometry. In addition, they differ in the number of size modes: P. obtusospinosa and P. rhea have two and P. tepicana has one. During colony ontogeny, P. obtusospinosa first has one mode and develops the second mode much later, while P. rhea produces multiple modes throughout. We also characterize worker caste systems based on the biomass allocation. For all three soldier-polymorphic species, the majority of soldiers are small soldiers. Pheidole obtusospinosa and P. rhea allocate roughly equal biomass to the two soldier classes, while P. tepicana allocates little to supersoldiers based on both biomass and caste ratio. These findings illustrate the interplay among caste ratios, biomass allocation, size frequency distributions, and allometry in the evolution of different worker caste systems. We conclude that soldier-polymorphic species may have evolved convergently in response to broad-scale factors, but differences among them suggest selection pressures in small-scale environments have been different.     

Castes in humivorous and litter-dwelling neotropical nasute termites (Isoptera,Termitidae)

Summary The developmental pathways of the neuter castes were studied in three species of Nasutitermitinae from central Panama. The humivorousSubulitermes denisae andCoatitermes clevelandi display several primitive traits: absence of sex dimorphism, representation of both sexes among workers and soldiers, and occurrence of successive worker instars. The litter-dwellingVelocitermes barrocoloradensis has a more complex caste system: female larvae are larger than males and give rise to the large workers, which constitute the bulk of the work force; male larvae proceed to soldiers through a small worker or a special larval instar. The resulting soldier caste is polymorphic. These results support previously formulated hypotheses regarding a link between humivorous diet and reduced polymorphism on the one hand, and between forest-floor foraging and large continuous size variation among soldiers on the other. Whereas the caste systems ofSubulitermes andCoatitermes probably represent a primitive condition,Velocitermes shares derived traits withNasutitermes and the other fully nasute genera previously studied. I therefore hypothesize that ancestors with these advanced features may have spread from the neotropics and be at the origin of most nasute genera, including humivorous taxa, present in other regions.     

八种白蚁的兵蚁和工蚁消化道形态比较研究(等翅目)

为探讨白蚁消化道形态品级差异及其系统学意义,对4个科8种白蚁兵蚁和工蚁的消化道进行比较形态学研究.结果表明:低等白蚁的兵蚁和(拟)工蚁形态较为相似,高等白蚁的兵蚁与工蚁局部特征存在明显差异.由低等到高等兵蚁和工蚁消化道各部分差异呈增多趋势.前、中、后肠占消化道的百分比在山林原白蚁Hodotermopsis sjoest...     

Male or female soldiers? An evaluation of several factors which may influence soldier sex ratio in lower termites

In termites, the soldiers’ sex ratio is often biased toward one sex. Unlike in the Hymenoptera, this bias cannot easily be explained by relatedness asymmetries because termites are diploid. Matsuura proposed that when large body size is adaptive for colony defence (e.g. in case of phragmotic defence) then the larger sex (given sexual size dimorphism exists) should be more likely to reach a threshold size and develop into soldiers. This would explain biased sex ratios. Matsuura validated his hypothesis for four Reticulitermes species. Here, we tested his hypothesis for two species of Cryptotermes with phragmotic defence. These drywood termites have a life type that is thought to be ancestral in termite’s evolution, thus giving us potential insights into the evolution of the soldier caste. In one of these species, the sex ratio of soldiers was highly female biased, but we could not support Matsuura’s hypothesis. Both species lacked sexual size dimorphism in all castes. Additionally, in both species, the sex ratio of helpers and sexuals did not deviate from a 1:1 ratio, and hence can also not account for the bias observed in soldiers. However, this study showed that there were behavioural differences between the sexes in both species, which could shed some light on biased sex ratio in soldiers. Our findings also indicate that the developmental pathway taken by individuals reflects a ‘decision’ at the colony level. The discovery of behavioural differences between sexes in termites should open the way to similar studies in other taxa with helpers/ workers of both sexes, as it might reveal more task partitioning in colonies than previously thought and it raises questions concerning the selective pressures that acted on caste evolution in termites. Received 30 October 2007; revised 17 January and 27 February; accepted 4 March 2008.     

尖唇散白蚁工蚁、兵蚁和繁殖蚁精子发生的比较研究

为探讨白蚁非生殖品级和生殖品级生殖细胞发育差异,采用组织学染色技术对尖唇散白蚁Reticulitermes aculabialis Tsaiet Hwang繁殖蚁、工蚁和兵蚁的精巢发育以及精子发生进行了显微观察和比较研究。结果发现3个品级间精巢发育的程度差异很大,三者精巢切面面积相对大小之比为:繁殖蚁∶工蚁=1.7∶1;繁殖蚁∶兵蚁=29.3∶1;工蚁∶兵蚁=17.1∶1。繁殖蚁和工蚁精巢管内有精子的形成,工蚁和繁殖蚁精子的发生都经历了精原细胞、初级精母细胞、次级精母细胞、精细胞和精子时期,但工蚁有大量次级精母细胞呈细胞凋亡状态。兵蚁生殖细胞发育仅有精原细胞、初级精母细胞、次级精母细胞,没有精细胞和精子产生。工蚁的生殖细胞显著小于同一时期繁殖蚁的生殖细胞,兵蚁的各时期生殖细胞均极显著小于繁殖蚁同一时期的生殖细胞。研究表明各品级之间生殖功能分化与生殖细胞发育有直接关系,工蚁有转化为补充繁殖蚁和兵蚁的能力;而兵蚁由于精巢极度退化不能产生精细胞和精子,因此是非生殖品级分化的终极形式,不具有转化成补充繁殖蚁或其它品级的能力。     

Studies on feeding and trophallaxis in the subterranean termite Odontotermes formosanus using rubidium chloride

Differences in feeding and trophallaxis among castes of the fungus‐cultivating higher subterranean termite Odontotermes formosanus Shiraki (Isoptera: Termitidae) were determined using rubidium (Rb) as a tracer. In the feeding study, workers and third instars fed directly on Rb‐treated filter paper and acquired the highest levels of Rb content. Although fifth and sixth instars obtained the Rb content over the marked level, the feeding ability of the caste was very poor. However, soldiers did not feed on Rb‐treated filter paper. In the trophallaxis study, worker, soldier, and fifth‐ and sixth‐instar recipients paired with Rb‐fed worker donors had a significantly higher Rb content than those paired with control donors. Results indicate that soldiers are completely dependent on workers for nutrition. Workers and fifth and sixth instars may obtain nutritional material from foraging workers. When third‐instar recipients were paired with Rb‐fed worker donors, they did not have a significantly higher Rb content than when they were paired with control donors, suggesting that the frequency of worker/third instar trophallaxis was very low. Transfer efficiency from the four trophallactic combinations ranged from 1.2 (worker donors to third‐instar recipients) to 12.9% (worker donors to soldier recipients). Accordingly, nutritional material from foraging workers could be transferred to non‐foraging workers, soldiers, and fifth and sixth instars by trophallaxis; however, third instars rarely obtain nutritional material from foraging workers, because they are capable of feeding within the nest.     

Worker aggression of ant Lasius japonicus enhanced by termite soldier–specific secretion as an alarm pheromone of Reticulitermes speratus

The subterranean termite Reticulitermes speratus usually nests in rotten wood trunks, which may also be occupied by the Japanese garden ant Lasius japonicus. Few battles were observed between them under ordinary circumstances because they inhabit separate nesting sites. However, once the termite nesting sites were artificially broken, the ant workers invaded and hunted the termites, although the termite soldiers fought against the ants. This study aims to confirm intra‐ and inter‐specific chemical interactions between the termite and ant. Solid phase microextraction–gas chromatograph (SPME‐GC) analyses revealed that R. speratus soldiers secreted caste‐specific sesquiterpene hydrocarbon when they were irritated. Both the hexane extract of the soldiers and its hydrocarbon fraction, as well as the crushed soldier bodies, attracted the soldiers but dispersed the workers when presented on the trails. We also confirmed that the soldier chemicals enhanced aggressiveness of L. japonicus, which rushed around the odor sources and hunted any termites that were present. These findings suggest that: (i) the soldier–specific secretion might serve as an alarm pheromone in termite chemical communication, in which components recruit soldiers and also warn the other colony members away; and (ii) termite communication is eavesdropped on by L. japonicus workers to locate and hunt the termites.     

Intra- and interspecific agonistic behavior of the subterranean termite Microcerotermes crassus (Isoptera: Termitidae)

The aim of our study was to investigate the intra- and interspecific agonistic behaviors exhibited by the worker and soldier castes of the subterranean termite Microcerotermes crassus Snyder (Isoptera: Termitidae). Aggression between M. crassus colonies from different field locations and also against three termite species--Coptotermes gestroi (Wasmann), Globitermnes sulphureus Haviland, and Odontotermes sp.--were observed in the laboratory. Termite responses were tested in paired combination of castes (soldiers versus soldiers, soldiers versus workers, and workers versus workers) consisting of 10 individuals each. Significant agonistic behaviors were observed only in encounters between pairings of different termite species. M. crassus was aggressive toward individuals from different species but not toward individuals from different M. crassus colonies. Mortality of M. crassus reached 100% in most of the interspecific encounters. However, no or low mortality was recorded in the intraspecific pairings.     

Soldier determination in Pheidole bicarinata: Effect of methoprene on caste and size within castes

Topical application of methoprene to final-instar larvae of the ant Pheidole bicarinata can induce soldier development. Soldier induction takes place if methoprene levels are above a soldier-determining threshold during a critical period of juvenile hormone-sensitivity that occurs during about days 4–6 of the final instar. Furthermore, the amount of exogenous methoprene applied affects the timing of metamorphosis and the adult size in both the minor worker and soldier castes. When larvae that receive methoprene treatment become minor workers these are always larger than acetone-treated controls. In larvae that become soldiers, growth and timing of metamorphosis vary with the dose of methoprene, but in a more complex way. A high dose of methoprene produces a metamorphic delay and large soldiers. However, the lowest effective dose for soldier induction produces early metamorphosis and small adults. On the basis of these results, we have expanded our model of a mechanism by which juvenile hormone could control determination of worker castes in Pheidole bicarinata.     

Caste differentiation responses of two sympatric <Emphasis Type="Italic">Reticulitermes</Emphasis> termite species to juvenile hormone homologs and synthetic juvenoids in two laboratory assays

Summary We report on our investigations comparing three juvenile hormone (JH) homologs and two synthetic juvenoids to induce caste differentiation in laboratory colonies of Reticulitermes flavipes and R. tibialis. Two laboratory assays were evaluated as model systems for inducing caste differentiation: (1) shorter-term dish assays on groups of 20 individuals and (2) longer-term feeding assays on groups of 500 individuals. Each assay possessed attributes that can be considered advantageous under certain conditions. Specifically, dish assays were most suitable for presoldier and soldier induction, while jar assays provided for the induction of nymphs, presoldiers, soldiers, neotenic reproductives, and intercastes. Differences in response to the JH homologs and synthetic juvenoids were noted between species, suggesting differences in JH physiology may exist between R. flavipes and R. tibialis. Substantial morpholo-gical impacts were noted in association with some treatments, including (1) juvenoid-induced mandibular mal-formation in presoldiers, (2) JH II-induced abdominal elongation in R. flavipes soldiers and workers (associated with a presence of internal reproductive anatomy that is consistent with what would be expected to occur in pseudergates), and (3) JH II-induced soldier-nymph intercastes in R. tibialis that were able to further molt into soldier-alate intercastes. Findings are discussed in relation to the potential differences in JH-related physiology between R. flavipes and R. tibialis, and the use of model systems to induce rare castes and intercastes for molecular investigations of caste differentiation.     

Soldier presence suppresses presoldier differentiation through a rapid decrease of JH in the termite Reticulitermes speratus

The regulation of caste differentiation is essential to insect eusociality. Termite soldiers are sterile and cannot eat by themselves because they have specialized mouth morphology. Almost all termite species have a soldier caste, and the soldier ratio per colony is maintained at a low level, probably by elaborate regulatory mechanisms. Although the soldier presence is considered to negatively affect soldier differentiation in all examined species, the detailed mechanism remains unclear. Presoldier differentiation can be induced artificially by juvenile hormone (JH) application to workers, showing that JH is a key factor underlying the regulation of soldier differentiation. In this study, to elucidate physiological changes in workers because of the soldier presence during the molt into presoldiers, JH III applications and JH titer quantifications were carried out in the rhinotermitid termite Reticulitermes speratus. Firstly, the effects of soldier presence before the molt into presoldiers induced by JH III application to workers were investigated. The rates of presoldier molt induced by the treatments with soldiers were significantly lower than those without soldiers. Secondly, worker JH titers in the presence or absence of soldiers were quantified by LC-MS on day 0, 5, 10, and 15 after JH application. Results indicated that the worker JH titers (endogenous + applied JH III) in the presence of soldiers were significantly lower than those without soldiers on day 5 after the JH treatment. On days 10 and 15, such soldier effects were not observed. Finally, the effective duration of soldier presence after the JH application was elucidated. A 4 day period of co-existence with soldiers suppressed presoldier differentiation, suggesting that the soldier presence rapidly decreased the JH titer in other colony members (i.e., workers), resulting in the inhibition of presoldier production.     

Nitrogen fixation in termites: Fate of newly fixed nitrogen

Nitrogen (¹⁵N) fixed by gut symbionts of the termite Nasutitermes corniger is assimilated and incorporated into termite tissues. Metabolic differences between soldier and worker castes are reflected in assimilation patterns: a greater proportion of the newly fixed nitrogen was in the bodies of workers but in the heads of soldiers. Newly fixed nitrogen is also transferred between workers and soldiers by trophallaxis. These studies confirm the 3:1 ratio assumed as the affinity of nitrogenase for acetylene relative to nitrogen in the acetylene-reduction method.     

Intracolonial differences in gut bacterial community between worker and soldier castes of Coptotermes formosanus

Abstract The establishment of symbiotic relationships with intestinal microorganisms enables termites to thrive on recalcitrant substrates such as cellulose and wood. A termite colony is composed of several different castes which have distinct feeding habits. The soldiers, for example, cannot feed by themselves and depend on workers, who feed them with digested or semi‐digested foods. To investigate the influence of feeding habits on the bacterial symbionts, a comparative study of gut bacteria between worker and soldier castes of the termite Coptotermes formosanus was conducted. The bacterial communities of both castes were investigated using denaturing gradient gel electrophoresis (DGGE) and clonal analysis of 16S ribosomal DNA (rDNA). Both methods indicated Bacteroidetes was the common predominant group; the common dominant phylotype was affiliated with a reported uncultured Bacteroidetes phylotype (BCf1–03). There were significant differences in Bacteroidetes and Spirochaetes between two castes. Compared to the gut bacteria of workers, those of soldiers were lower in abundance and diversity of Bacteroidetes and slightly higher in Spirochaetes. Two phylotypes (W8, W11) affiliated to Bacteroidetes and two (W26, W29) affiliated to Spirochaetes were exclusively found in the DGGE profile of the worker caste. Bacteroidetes are assumed to be involved in fermentation of sugars and nitrogenous compounds as well as degradation of uric acid. Spirochaetes are supposed to aid in the functions of acetogenesis and N₂‐fixation. The different feeding habits between workers and soldiers of C. formosanus may explain the observed differences in the gut bacterial community.     

Endogenous synchronization of the chemical signature of Reticulitermes (Isoptera: Rhinotermitidae) worker termites

Termites of the genus Reticulitermes are characteristic of temperate regions. Their colonies comprise various castes, the most numerous being that of workers which can develop into soldiers or secondary reproductives (neotenics). Each caste has a mixture of hydrocarbons (HCs) on the cuticle forming a chemical signature. The primary aim of this study was to compare the changes in the chemical signature of a population of worker termites fed on paper with juvenile hormone to differentiate them into soldiers with a control population of termites fed only on paper or wood for one month. Gas chromatography was used to analyze the cuticular profiles of Reticulitermes flavipes termites to determine whether they changed, and, if so, when and how. The data collected over one month showed that the workers fed with JH did not differentiate into soldiers but that there were progressive changes in the hydrocarbon profile independent of the treatment. These results indicate that the differentiation of the chemical signature of the worker caste is a dynamic process, depending only on time and not on colony membership, confirming that, for these termites, this signature has a lesser role in colony membership than caste membership, unlike the chemical signatures of other social insects. The temporal process of this cuticular change is also associated with a change in the alkene/methyl-branched alkane ratio.     

Cuticular Hydrocarbons of Reticulitermes (Isoptera: Rhinotermitidae) from Northern California Indicate Undescribed Species

Cuticular hydrocarbon mixtures of Reticulitermes samples from disparate locations in northern California were characterized and correlated with species determinations. Literature records indicate that there are two extant species of Reticulitermes in northern California: Reticulitermes hesperus Banks and R. tibialis Banks. We identified five distinct hydrocarbon phenotypes in Reticulitermes from northern California. Termites were diagnosed morphologically as R. tibialis for all five cuticular hydrocarbon phenotypes based on available keys to soldiers. Commonly accepted distributions of Reticulitermes in northern California indicate that our primary collection sites should only produce R. hesperus. On the basis of cuticular hydrocarbons alone we suggest that there are two or more undescribed taxa of Reticulitermes in northern California, or that described species of Reticulitermes occur in northern California, but have never been noticed before. Therefore, we conclude that the taxonomy of Reticulitermes in North America is in need of revision.