Asexual queen succession in the higher termite Embiratermes neotenicus

Asexual queen succession (AQS), in which workers, soldiers and dispersing reproductives are produced sexually while numerous non-dispersing queens arise through thelytokous parthenogenesis, has recently been described in three species of lower termites of the genus Reticulitermes. Here, we show that AQS is not an oddity restricted to a single genus of lower termites, but a more widespread strategy occurring also in the most advanced termite group, the higher termites (Termitidae). We analysed the genetic structure in 10 colonies of the Neotropical higher termite Embiratermes neotenicus (Syntermitinae) using five newly developed polymorphic microsatellite loci. The colonies contained one primary king accompanied either by a single primary queen or by up to almost 200 neotenic queens. While the workers, the soldiers and most future dispersing reproductives were produced sexually, the non-dispersing neotenic queens originated through thelytokous parthenogenesis of the founding primary queen. Surprisingly, the mode of thelytoky observed in E. neotenicus is most probably automixis with central fusion, contrasting with the automixis with terminal fusion documented in Reticulitermes. The occurrence of AQS based on different mechanisms of ploidy restoration raises the hypothesis of an independent evolutionary origin of this unique reproductive strategy in individual lineages of lower and higher termites.     

On the origin of termite workers: weighing up the phylogenetic evidence

Resolving the phylogenetic history of a 'true' worker caste in termites is essential to our understanding of termite eusocial evolution. Whether this caste is ancient and monophyletic or derived and polyphyletic will have a tremendous impact on our interpretation of termite eusocial history and remains an outstanding question in termite biology. Recent work has begun to re-examine this question in light of new phylogenetic information, but new questions have now arisen about how best to model character state changes in termite caste systems. In the present paper, we compare the models of Grandcolas and D'Haese [J. Evol. Biol. 15 (2002) 885] and Thompson et al. [J. Evol Biol. 13 (2000) 8691 and attempt to make explicit how these proposals differ with respect to the number of, and homology between, character states. We highlight the support each model has for the two principal, but competing, evolutionary hypotheses outlined above.     

Intraspecific variation in soldier defense secretions of Longipeditermes longipes (Isoptera,Nasutitermitinae)

The chemical defense secretions of major and minor soldiers of 46 colonies of the free-ranging termite Longipeditermes longipes (Isoptera, Termitidae, Nasutitermitinae) were isolated and analyzed by chromatography and spectroscopy. The colonies, collected from rainforest sites in Malaysia, showed monoterpene patterns rich in pinenes and limonene but with few qualitative differences among colonies. In marked contrast, the diterpene chemistry is highly variable that includes bicyclic (secotrinervitane), tricyclic (trinervitane), tetracyclic (rippertane), and a spirotetracyclic (longipane) skeleton. This paper presents the compositional and structural diversity, and calculates genetic distances among sympatric and allopatric colonies from a single species.     

Caste developmental potentialities in the termite Nasutitermes novarumhebridarum

The normal development pathway and caste system of Nasutitermes novarumhebridarum (N. & K. Holmgren) (Isoptera; Termitidae) conform to the general Nasutitermes pattern. Queen-removal experiments in N. novarumhebridarum resulted in the production of replacement reproductives derived from workers (ergatoids), but never from the sexual brood (nymphs and alates). Three moults are necessary to complete the tranformation from the worker to the ergatoid. This pathway is longer than those previously konwn in other termites, in which two moults are sufficient. In a colony with functional ergatoids, some nymphs gave rise to worker-like individuals. The caste potentialities of N. novarumhebridarum differ from those of the sympatric species, N. princeps and N. polygynus, in which imaginal replacement reproductives are easily obtained. Colony reproduction in N. novarumhebridarum seems to be accomplished exclusively by independent alate founders, which colinize massive, but finite and widely spaced resoures such as dead or damaged tree trunks. N. princeps and N. polygynus societies abundantly use colony budding to expand their territory, and exploit various sources of dead wood scattered over their foraging range. We suggest that N. novarumhebridarum caste potentialities are adapted to channelling a maximum of resources into the production of dispersing alates that can colonize new nest sites.

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Résumé Les voies de développement et le système de castes chez Nasutitermes novarumhebridarum sont conformes au schéma général du genre Nasutitermes. L'enlèvement expérimental de la reine chez N. novarumhebridarum entraîne le développement de sexués de remplacement à partir d'ouvriers (ergatoïdes), mais jamais à partir de la lignée sexuée (nymphes et ailés). La transformation de l'ouvrier en ergatoîde fonctionnel nécessite trois mues. Ce développement est plus long que ceux décrits précédemment chez d'autres termites, où deux mues sont suffisantes. Dans une société où se sont développés des ergatoïdes fonctionnels, quelques nymphes se sont transformées en individus rappelant les ouvriers. Les potentialités des castes de N. novarumhebridarum diffèrent de celles des espèces sympatriques N. princeps et N. polygynus, chez lesquelles des sexués de remplacement imaginaux pauvent être obtenus aisément. La reproduction des sociétés de N. novarumhebridarum semble s'effectuer uniquement par des ailés essaimants, qui colonisent des sources de nourriture massives, mais limitées et largement espacées, tels les troncs d'arbres morts ou endomagés. N. princeps et N. polygynus étendent fréquemment leurs territoires par le bourgeonnement de nouvelles sociétés, et exploitent des sources de bois mort variées, dispersées dans leur champ d'exploitation. Nous suggérons que les potentialités des castes chez novarumhebridarum sont adaptées pour diriger un maximum de ressources vers la production d'ailés qui se dispersent et peuvent ainsi coloniser de nouveaux sites favorables.

     

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.     

Polymorphism in the giant cocoa termite,Neotermes papua (Desneux)

Summary The direct development ofNeotermes papua (Isoptera: Kalotermitidae) comprises four larval and three nymphal instars before the alate. The first five instars can be easily characterized. The second stage nymphs come morphologically close to the pseudergates, characterized by reduced wing buds. These nymphs can moult stationarily, i.e. with little morphological change, or to presoldiers, or proceed to the alate via the third nymphal stage. Pseudergates originate through a late and reversible deviation from the straight development to the alate. Presoldiers may derive from several stages, up to the last nymphal one; their production is subject to an inhibition by extant soldiers. This developmental schema is congruent with those described in other Kalotermitidae and the Termopsidae. By pinpointing the existence of a large pool of pluripotent individuals, in which the penultimate nymphal stage mingles with pseudergates, the present study also reveals a great similarity betweenNeotermes andProrhinotermes, and suggests that this developmental schema might be generally applicable to termites devoid of a permanent worker caste.King Léopold III Biological Station, Laing Island, Papua New Guinea, contribution No. 235     

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.     

Polymorphism in the neotropical termite Serritermes serrifer

Serritermitidae (Isoptera) is a small and little known Neotropical termite family which includes only two genera: Glossotermes and Serritermes. Despite the lack of detailed studies, it has been assumed that these termites have a true worker caste. A recent study revealed that Glossotermes has a linear development pathway and lacks true workers. Here, we present a study of the polymorphism of Serritermes serrifer Hagen & Bates, a species endemic to the Cerrado ecoregion of central Brazil which lives as an inquiline inside nests of Cornitermes spp. A morphometric analysis was performed based on measurements taken of 11 body parts of 544 specimens of immatures, worker‐like individuals, soldiers, and alates. Sex of specimens was determined by dissection and examination of the seventh sternite. A principal component analysis (PCA) was used to evaluate morphological changes during development. Contrary with previous information from the literature and similar to Glossotermes, Serritermes shows a linear development pathway with two larval instars, two sizes of pseudergates, and a single nymphal morph. Pseudergates apparently undergo stationary molts. Sex ratio among pseudergates is male‐biased, but not as strongly as in Glossotermes. Typical colonies have a single physogastric primary queen and a single primary king. Ergatoid reproductives are relatively rare and some female ergatoids may become strongly physogastric. Nymphoid reproductives were not found. All soldiers are male and bear well‐developed testes.     

Isolation and characterization of microsatellite markers in Labiotermes labralis (Isoptera,Termitidae, Nasutitermitinae)

We report here on the development of six polymorphic microsatellite loci for Labiotermes labralis. This soil‐feeding species is restricted to the Neotropical rainforest and then could represent a major candidate for being a bio‐indicator of anthropic disturbance resulting in the forest fragmentation. The microsatellite loci were isolated and characterized using a microsatellite‐enriched genomic library. The primers were tested on a French Guyanese population of L. labralis, represented by the sampling of one soldier in 22 nests. The primers were also tested against nine species of the same Nasutitermitinae subfamily and were successfully amplified at five loci in Armitermes minutus.     

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.     

Microsatellite markers for the polygamous termite Nasutitermes corniger (Isoptera: Termitidae)

We developed eight highly variable microsatellite markers for the termite Nasutitermes corniger. Allele number per locus ranged from nine to 34, and expected heterozygosity from 0.45 to 0.94, in samples from seven sites in the former canal zone of Panama. The utility of these markers was assessed for five congeners varying in phylogenetic distance to N. corniger. The markers will be useful for fine‐scale examination of population and colony genetic structure in N. corniger and other closely related species.     

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

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

Growth and demography ofCubitermes speciosus mounds (Isoptera,Termitidae)

The growth and demography ofCubitermes speciosus mounds were studied in an equatorial forest ecosystem near Kisangani, Zaïre. The mounds were censused and measured on eight occasions from June 1985 to January 1993 on 25 plots of 100 m².Mounds were found to grow in two ways: either they were enlarged sporadically, leading to a correlation between age and size; or they were no longer enlarged after a 2-year period of initial growth, which means that both large and small mounds can be old.The number of living mounds was fairly constant: it varied between 112 and 152 ha^–1 with an average of 139 ha^–1, and about a quarter of them were renewed each year. However, a clear tendency was observed over our 7.5-year observation period: the average size of the mounds increased regularly and was 2.7 times larger in 1993 than in 1985.Monthly birth and death rates were estimated using a model of continuous growth. Life expectancy at the age of 3 months was estimated from a survivorship curve at 3.5 years.     

Development of physogastry in the queen of the fungus-growing termite Macrotermes michaelseni (Isoptera: Macrotermitinae)

Female reproductives of the fungus-growing termite Macrotermes michaelseni never showed signs of physogastry if they were kept in petri dishes to establish an incipient colony. During the 200 days of observation, their corpora allata volume, juvenile hormone titre and number of active ovarioles remained on a more or less constant level, and their gut was filled with soil. In contrast, these parameters are enhanced in partially and especially in fully physogastric queens, and these females had only a transparent liquid in the gut.Application of the juvenile hormone mimic ZR 515 to young females accelerated yolk incorporation, increased the number of active ovarioles and brought about the release of the soil from the gut. The same changes were induced by adding workers to increase the population of incipient colonies from about 45 to 400. This also resulted in an increase of the corpus allatum volume and of the juvenile hormone titre in young females. Their intestine was in this case filled with transparent liquid associated with the increased population of workers. It was, therefore, concluded that the development of physogastry depends on a positive feedback: the more workers are with the young female, the more nutrients are available and the more juvenile hormone the female produces, the more eggs are laid and the more workers can again develop to nurture the queen.     

Chemotaxonomy of Subulitermes and Nasutitermes termine soldier defense secretions. Evidence against the hypothesis of diphyletic evolution of the Nasutitermitinae

The soldier defense secretions of advanced neotropical termites of the genus Subulitermes (Isoptera, Nasutitermitinae) contain diterpenes identicalto those found in Nasutitermes species, while soldiers of the primitive mandibulate nasute genera Cornitermes, Armitermes and Rhynchotermes lack diterpenoid compounds. It now appears improbable that the elongate nasus and intimately associated terpenoid defense secretions evolved from a primitive mandibulate ancestor independently along two phyletic branches. An alternate hypothesis is proposed in which morphological divergence from a common diterpene-producing ancestor may have occurred.     

黑胸散白蚁幼期不同品级的发育和分化

在黑胸散白蚁Reticulitermes chinensis发育和分化过程中,发现有假工蚁、假若蚁两种虫态。假工蚁由6龄和7龄工蚁转化发育而来,假若蚁由4龄和5龄若蚁转化发育而来。显微测量结果表明,黑胸散白蚁的胚后发育主要包括2个龄期的幼蚁期、6个以上龄期的工蚁期、4个龄期的若蚁期和有翅成虫。在此基础上分析了其他虫态的分化来源,发现兵蚁由3～7龄工蚁分化发育而来,翅鳞型和长翅芽型补充生殖蚁由6龄若蚁转化发育而来,短翅芽型补充生殖蚁由4龄和5龄若蚁转化发育而来,微翅芽型补充生殖蚁既可由4～6龄工蚁转化发育而来,又可由假工蚁和假若蚁转化发育而来,无翅型补充生殖蚁由3～7龄工蚁转化发育而来。提出了黑胸散白蚁群体中不同品级个体的可能分化途径。     

黑胸散白蚁幼期不同品级的发育和分化

在黑胸散白蚁Reticulitermes chinensis发育和分化过程中,发现有假工蚁、假若蚁两种虫态。假工蚁由6龄和7龄工蚁转化发育而来,假若蚁由4龄和5龄若蚁转化发育而来。显微测量结果表明,黑胸散白蚁的胚后发育主要包括2个龄期的幼蚁期、6个以上龄期的工蚁期、4个龄期的若蚁期和有翅成虫。在此基础上分析了其他虫态的分化来源,发现兵蚁由3～7龄工蚁分化发育而来,翅鳞型和长翅芽型补充生殖蚁由6龄若蚁转化发育而来,短翅芽型补充生殖蚁由4龄和5龄若蚁转化发育而来,微翅芽型补充生殖蚁既可由4～6龄工蚁转化发育而来,又可由假工蚁和假若蚁转化发育而来,无翅型补充生殖蚁由3～7龄工蚁转化发育而来。提出了黑胸散白蚁群体中不同品级个体的可能分化途径。     

Queen replacement in the termiteMicrocerotermes papuanus

In experimentally orphaned field nests ofMicrocerotermes papuanus Holmgren, 1911, large numbers of workers develop into replacement reproductives (ergatoids) in only one moult. The females become functional egg-layers after approximately two months. Nymphs normally reach the last instars in August–September; at that time, in the orphaned nests, some nymphs moult to nymphoid replacement reproductives. Over long time periods, these nymphoids completely replace the ergatoids and the females become physogastric. Although time-efficient, queen replacement seems energetically expensive for the society, suggesting that this process is under weak selective pressure inM. papuanus, compared with sympatric species such asNasutitermes princeps.

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Le remplacement de la reine chez le termiteMicrocerotermes papuanus

Résumé Dans les nids deM. papuanus rendus expérimentalement orphelins, un grand nombre d'ouvriers se transforment, en une seule mue, en sexués de remplacement ergatoïdes. Les femelles se mettent à pondre au bout d'environ deux mois. Les nymphes atteignent normalement leurs derniers stades en août-septembre. A ce moment, dans les nids orphelins, certaines d'entre elles se différencient en sexués nymphoïdes. Dans les expériences de longue durée, ces nymphoïdes remplacent complètement les ergatoïdes et les femelles deviennent physogastres. Bien que rapide, le remplacement de la reine paraît coûteux pour la société du fait du grand nombre d'individus, ouvriers et nymphes, impliqués. Ceci suggère que la pression de sélection sur ce phénomène est faible chezM. papuanus, par comparaison avec des espèces sympatriques telles queN. princeps.