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.     

The origin of a ‘true’ worker caste in termites: phylogenetic evidence is not decisive

The phylogenetic study of the origin of a ‘true’ worker caste in termites by Thompson et al. [J. Evol. Biol. 13 (2000) 869] did not take into account all possibilities of character coding and character optimization on the phylogenetic tree. Actually, contrary to the authors' statements, the phylogenetic evidence presented does not permit to answer decisively most of the questions asked concerning the origin and evolution of worker castes in termites. Particular attention was paid to assumptions implied by the coding of the characters of interest, namely concerning the homology between pseudergates and a ‘true’ worker caste and the kind of the cockroach life type.     

Winged presoldiers induced by a juvenile hormone analog in Zootermopsis nevadensis: implications for plasticity and evolution of caste differentiation in termites

To elucidate the switching mechanism of caste differentiation in termites and to examine the possible induction of soldier-reproductive intercastes experimentally, we investigated the effects of juvenile hormone on the morphologies of soldier caste by applying a juvenile hormone analog (JHA) to nymphs of the damp-wood termite Zootermopsis nevadensis (Isoptera : Termopsidae). JHA treatment for about 2 weeks induced a variety of intermediate castes, showing both alate and soldier morphological features. The principal component analysis (PCA) of those morphological characters showed that those intercastes were a deviation from the developmental line into alates to soldier differentiation, which is known to be triggered by juvenile hormone. Detailed morphological examination of the compound eyes, wing joint, and mandibles showed that those intercastes expressed soldier features, although they had started to develop alate characteristics. The morphology of the resultant intercastes seemed to be determined by the nymphal stage, at which JHA treatment was applied. The induced intercastes with exaggerated soldier-specific characteristics (e.g., mandibles) repressed alate-specific characteristics (e.g., wings), namely, the alate and soldier morphological characteristics in induced intercastes show opposite responses against the application of JHA. On the other hand, ovarian development was not suppressed by the JHA application, even in the soldier-like individuals. Naturally differentiated presoldiers also possessed developed ovarioles, although ovaries of mature soldiers were degenerated. Our results suggest that the juvenile hormone plays complicated roles in the expression of caste morphologies and ovarian development in termites.     

Phylogenetic evidence for a single,ancestral origin of a ‘true’ worker caste in termites

Phylogenetic analysis based on sequence variation in mitochondrial large‐subunit rRNA and cytochrome oxidase II genes was used to investigate the evolutionary relationships among termite families. Maximum likelihood and parsimony analyses of a combined nucleotide data set yield a single well‐supported topology, which is: (((((Termitidae, Rhinotermitidae), Serritermitidae), Kalotermitidae), (Hodotermitidae, Termopsidae)), Mastotermitidae). Although some aspects of this topology are consistent with previous schemes, overall it differs from any published. Optimization of ‘true’ workers onto the tree suggests that this caste originated once, early in the history of the lineage and has been lost secondarily twice. This scenario differs from the more widely accepted notion that workers are derived and of polyphyletic origin and that extant pseudergates, or ‘false’ workers, are their developmentally unspecialized ancestor caste. Worker gains and losses covary directly in number and direction with shifts in ‘ecological life type’. A test for correlated evolution which takes phylogenetic structure into account indicates that this pattern is of biological significance and suggests that the variable occurrence of a worker caste in termites has ecological determinants, apparently linked to differences in feeding and nesting habits.     

Evolution of eusociality and the soldier caste in termites: a validation of the intrinsic benefit hypothesis

In termites the evolution of reproductive altruism is not based on a particularly high relatedness between nestmates. For the evolution and maintenance of the ancestral sterile soldier caste, the benefits generated by the soldiers' presence must compensate the loss of the soldiers' reproductive potential. To study the impact of soldiers on colony's fitness, we manipulated the proportion of soldiers to nonsoldiers in colonies of the dry-wood termite Cryptotermes secundus.'Soldier-less' colonies were obtained by removing soldiers and inhibiting their development with an extract of soldier heads. The colonies were set up for 1 year in experimental nests in the field. 'Soldier-less' colonies produced fewer soldiers. The reduction of soldiers neither affected colony survival nor helper growth, but fewer dispersing sexuals were produced in 'soldier-less' than in control colonies. This confirms what was only supposed so far, that in termites soldiers are maintained for their intrinsic benefit to cost ratio.     

Evidence for genetically influenced caste determination in phylogenetically diverse species of the termite genus Reticulitermes

A number of social insect species have recently been shown to have genetically influenced caste determination (GCD), challenging the conventional view that caste determination should be strictly environmental. To date, GCD has been found in phylogenetically isolated species; examples of GCD being present in multiple species of a genus are lacking. Through crossing experiments of neotenic (juvenile) reproductives, we have recently provided the first evidence for a royal versus worker GCD in the termite Reticulitermes speratus. To elucidate whether this system is more widespread, we performed crossing experiments using three additional Reticulitermes species. Offspring caste and sex ratios were found to be highly similar to those found previously in R. speratus, raising the possibility that GCD was present in an ancestral lineage of Reticulitermes, and subsequently maintained throughout several episodes of speciation.     

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.     

The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: Implications for the evolution of the worker and pseudergate castes, and foraging behaviors

A phylogenetic hypothesis of termite relationships was inferred from DNA sequence data. Seven gene fragments (12S rDNA, 16S rDNA, 18S rDNA, 28S rDNA, cytochrome oxidase I, cytochrome oxidase II and cytochrome b) were sequenced for 40 termite exemplars, representing all termite families and 14 outgroups. Termites were found to be monophyletic with Mastotermes darwiniensis (Mastotermitidae) as sister group to the remainder of the termites. In this remainder, the family Kalotermitidae was sister group to other families. The families Kalotermitidae, Hodotermitidae and Termitidae were retrieved as monophyletic whereas the Termopsidae and Rhinotermitidae appeared paraphyletic. All of these results were very stable and supported with high bootstrap and Bremer values. The evolution of worker caste and foraging behavior were discussed according to the phylogenetic hypothesis. Our analyses suggested that both true workers and pseudergates (“false workers”) were the result of at least two different origins. Our data support a traditional hypothesis of foraging behavior, in which the evolutionary transition from a one-piece type to a separate life type occurred through an intermediate behavioral form.     

The role of exogenous JH I,JH III and Anti-JH (precocene II) on queen induction of 4.5-day-old worker honey bee larvae

Worker larvae at an age of 4½ days were fed one of several mixtures of reconstituted royal jelly adjusted to a refractive index of 1.3825 and supplemented with JH I, JH III or Anti-JH (precocene II). In addition, juvenile hormone was topically applied to larvae of the same age. It was readily apparent that caste induction is concentration-dependent and that 4?-day-old worker larvae can still develop into queens under laboratory conditions, providing that they have not stopped feeding or can be induced to commence feeding again. These findings are contrary to the general belief that queen induction is not possible after a socalled sensitive period of 3–3½ days. Queens resulted only from honey bee larvae exposed to royal jelly containing 1 μg of JH I. In addition, oral application at this concentration resulted in the only case in which the normal mean weights of worker honey bees were exceeded. All other concentrations of juvenile hormone were not sufficient to initiate queen induction, although its lower concentration may have influenced the production of intercastes.Precocene II did not play a role in queen induction and it also did not interfere with the growth of developing larvae or adults. In addition, the lack of malformations in honey bees treated with precocene II indicates that the use of such a compound as a control agent in insect populations will probably not be detrimental to honey bee larvae that are at least 4½ days old. However, large doses of precocene will quickly kill most 3½-day-old honey bee larvae.The evidence presented here clearly indicates that caste determination is regulated by the endocrine system in honey bee larvae. Food intake in honey bee larvae may well be regulated by the endocrine system. Thus, an apparently inhibited corpus allatum (C.A.) could be reactivated by food intake coupled with juvenile hormone. The food intake restriction that worker larvae normally encounter in the hive probably results in a cessation of C.A. activity. The increase in food intake by queen larvae, on the other hand, carries an increase in growth and accompanying morphological changes necessary for queen development. This concept may also explain the development of intercastes encountered in in vitro studies. Only those larvae that follow a normal food intake sequence, i.e. moderate during the first 3–4 days or so, will develop into queens. Conversely, those larvae that take in too much food during the early portion of development may achieve incomplete development of the neurosecretory system and, thus, develop into intercastes.     

Levels of specificity of Xylaria species associated with fungus-growing termites: a phylogenetic approach

Fungus-growing termites live in obligate mutualistic symbiosis with species of the basidiomycete genus Termitomyces , which are cultivated on a substrate of dead plant material. When the termite colony dies, or when nest material is incubated without termites in the laboratory, fruiting bodies of the ascomycete genus Xylaria appear and rapidly cover the fungus garden. This raises the question whether certain Xylaria species are specialised in occupying termite nests or whether they are just occasional visitors. We tested Xylaria specificity at four levels: (1) fungus-growing termites, (2) termite genera, (3) termite species, and (4) colonies. In South Africa, 108 colonies of eight termite species from three termite genera were sampled for Xylaria . Xylaria was isolated from 69% of the sampled nests and from 57% of the incubated fungus comb samples, confirming high prevalence. Phylogenetic analysis of the ITS region revealed 16 operational taxonomic units of Xylaria , indicating high levels of Xylaria species richness. Not much of this variation was explained by termite genus, species, or colony; thus, at level 2–4 the specificity is low. Analysis of the large subunit rDNA region, showed that all termite-associated Xylaria belong to a single clade, together with only three of the 26 non-termite-associated strains. Termite-associated Xylaria thus show specificity for fungus-growing termites (level 1). We did not find evidence for geographic or temporal structuring in these Xylaria phylogenies. Based on our results, we conclude that termite-associated Xylaria are specific for fungus-growing termites, without having specificity for lower taxonomic levels.     

Developmental pathways of Glossotermes oculatus (Isoptera, Serritermitidae): at the cross-roads of worker caste evolution in termites

SUMMARY The onset of a specialized ("true") worker caste is a crucial step in the evolution of termite societies. Such workers, permanently excluded from wing development, repeatedly evolved from totipotent immatures, called "false" workers or pseudergates. In the family Rhinotermitidae, the presence of true workers and the level of specialization of this caste are highly variable, and key taxa illustrate transitional situations providing clues about worker evolution. Here we focused on the status of working immatures of Glossotermes oculatus , from the family Serritermitidae, now thought to represent either the sister-group of the Rhinotermitidae or a basal lineage nested within them. Contrary to previous assumptions, we show that the apterous immatures performing worker tasks in G. oculatus are the source of the single wing-budded nymphal instar preceding the alate. Consequently, they qualify as pseudergates rather than true workers. However, the sex ratio is strongly male biased in pseudergates and soldiers, which is a trait usually restricted to termites with true workers. We therefore argue that pseudergates of G. oculatus are close to a point where the species could easily shift toward the differentiation of a true worker caste, and that G. oculatus pinpoints a new possible route for the evolution of true workers from pseudergates.     

白蚁肠道共生微生物的作用:酵母,一个“隐身”的特别菌群

长期以来,白蚁对木质纤维素的降解能力令人惊叹,毫无疑问,其在全球碳循环中扮演着一个十分重要的角色。这一强大功能的实现极大地依赖于一种特别的肠道"消化液(digestome)",它的构成不仅包括了来自白蚁自身产生的木质纤维素降解酶系统,还来源于独特与多样的肠道共生微生物的贡献(包括了古细菌、细菌、酵母以及其他真核生物),它们的协同作用能有效地将木质纤维素生物质高效转化为乙酸、甲烷、二氧化碳、氢气等物质。然而,到目前为止,我们对这类昆虫的独特肠道生物转化系统的认识还很不深入,特别是针对肠道内的那些各类共生微生物菌群的功能、白蚁与共生微生物间的相互关系、以及潜在的科学与应用价值还无法给予明确的科学解释,更不用说针对其肠道中的共生酵母菌群,一类通常被忽略的独特微生物。近20多年来,越来越多的研究证据表明,白蚁肠道共生酵母在与寄主的关系中表现了不可或缺的重要性与独特功能,已被证明广泛分布于不同白蚁及许多其他昆虫的肠道中。随着近20年来越来越多昆虫肠道共生微生物酵母群被发现和鉴定,他们潜在的功能以及与寄主的共生机制被逐步解析,这些研究结果进一步揭示了"隐身"的昆虫肠道酵母类微生物菌群与寄主的营养、关键生物质转化过程中的重要酶系统、转化过程中的关键中间产物的转化与利用、抵御外源性的重要病原物,甚至对白蚁种群繁衍的远缘交配等方面均可能发挥了重要和不可缺少的作用。本文将试图归纳相关研究的最新进展,系统总结与解析白蚁肠道来源共生酵母的重要科学价值及其在不同领域的潜在应用前景。     

Testing the importance of the distribution of worker sizes to colony performance in the ant species <Emphasis Type="Italic">Formica obscuripes</Emphasis> Forel

We examined the relationship between colony performance and the distribution of worker sizes within colonies in the ant species, Formica obscuripes. We manipulated the distribution of worker sizes within colonies and found that experimental colonies whose distributions mimicked the natural distributions retained a larger percentage of colony biomass over three weeks when fed on honeydew, relative to colonies composed of only large or only small workers. In natural colonies most of the variation in worker sizes was found within, as opposed, to between colonies, suggesting that homeostatic mechanisms within colonies regulated the distribution of worker sizes. While there were no disjunctions in the distribution of worker sizes within colonies, the distribution tended to be bimodal. This study demonstrates that the distribution of worker sizes within colonies is important even for ant species that lack discrete worker castes. Received 31 October 2006; revised 26 December 2006; accepted 4 January 2007.     

The effect of nonnestmates on foraging trail caste ratios ofNasutitermes corniger (Isoptera: Termitidae)

The mean number of workers on foraging trails ofNasutitermes corniger Motschulsky decreases after the introduction of nonnestmate conspecifics or congeneric heterospecifics. The mean number of soldiers on foraging trais does not vary when nestmates, conspecific nonnestmates or heterospecific workers are introduced. When heterospecific soldiers are introduced to the trail, however, the number ofN. corniger soldiers increases. Consequently, the ratio of soldiers to workers increases. These findings demonstrate that the addition of nonnestmates temporarily alters caste ratios on foraging trails, representing a shift in the distribution of castes in response to environmental perturbation.     

Myths of meritocracy: caste,karma and the new racism,a comparative study

The discourse of karma (behaviour), confounded with inherent psychic and material substance of the person/group (guna), was at the heart of India’s caste ideology. This systematic and intuitive, albeit convoluted and phantasmic doctrine was critical to bridge the discrepancy between a pantheistic religious imaginary and the reality of exclusion and abjection. Although “karma” evokes an exotic orient, this ideology is near identical with the ideas of “idleness” and “instant gratification” used to make sense of racial inequities in the contemporary United States. In both cases, the idea of behavioural and moral deficiency is used to justify evident abjection and discrimination, within the frame of an encompassing ideology of social equality. Thus, this use of the notions of “work” and “discipline”, extrapolated to the moral quality of the group or individual, is no passing argument of the “new racism”. It is a proven ploy of assigning blame on the victim.     

The phylogenetic position of the Clitellata and the Echiura - on the problematic assessment of absent characters*

Absent characters (negative characters) are difficult to assess and their correct interpretation as symplesiomorphies, synapomorphies or convergencies (homoplasies) is one of the greatest challenges in phylogenetic systematics. Different phylogenetic assessments often result in contradictory phylogenetic hypotheses, in which the direction of evolutionary changes is diametrically opposed. Especially in deciding between primary (plesiomorphic) and secondary (apomorphic) absence, false conclusions may be reached if only the outgroup comparison and the principle of parsimony are employed without attempting any biological evaluation or interpretation of characters. For example, in the higher‐level systematization of the Annelida and related taxa different assessments of absent characters have led to conflicting hypotheses about the phylogenetic relationships and the ground pattern of the annelid stem species. Varying phylogenetic interpretations regarding the absence of the chemosensory nuchal organs in the clitellates and their presence in polychaetes initiated a controversy that produced two alternative phylogenetic hypotheses: (1) the Clitellata are highly derived Annelida related to a subtaxon within the, in this case, paraphyletic ‘Polychaeta’ or (2) the Clitellata are comparatively primitive Annelida representing the sister group of a monophyletic taxon Polychaeta. In the former, the absence of nuchal organs in the Clitellata is regarded as a secondary character, in the latter as primary. As most Clitellata are either limnetic or terrestrial, we must ask which characters are plesiomorphies, taken from their marine stem species without changes. In addition to a thorough investigation and evaluation of clitellate characters, a promising approach to these questions is to look for such characters in limnetic and terrestrial annelids clearly not belonging to the Clitellata. A similar problem applies to the evaluation of the position of the Echiura, which lack both segmentation and nuchal organs. Evidence is presented that in both taxa these absent characters represent derived, apomorphic character states. The consequences for their phylogenetic position and the questionable monophyly of the Polychaeta are discussed. The conclusion drawn from morphological character assessments is in accordance with recently published hypotheses based on molecular data.     

Temporal polyethism in incipient colonies of the primitive termiteZootermopsis angusticollis: A single multiage caste

Division of labor was studied in incipient colonies of the dampwood termite Zootermopsis angusticollisby recording repertoire size, behavior frequencies, and time budgets of larvae. Behavioral repertoire size increased with age: first- and secondinstar larvae were mainly inactive, whereas larvae of the third through seventh instars performed 64–100% of all tasks. The increase in repertoire size from the second to the third instar was abrupt; repertoire size and composition remained more or less constant for older instars. No correlation between age (instars III–VII) and tasks was identified, suggesting that colony labor is performed by a single functional caste that spans the third to the seventh instar without any age-based division of labor. Small colony size, low oviposition rate, simple nest architecture, a lack of spatial association of tasks, and the potential for attaining reproductive status appear to be associated with the lack of age-related behavioral specialization in Z. angusticollis.In effect, the absence of temporal polyethism in this species is likely a consequence of its nesting habits and physiological and developmental constraints.     

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton''s rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.     

Why join a neighbour: fitness consequences of colony fusions in termites

The evolution of life is characterized by major evolutionary transitions during which independent units cooperated and formed a new level of selection. Relatedness is a common mechanism that reduces conflict in such cooperative associations. One of the latest transitions is the evolution of social insect colonies. As expected, they are composed of kin and mechanisms have evolved that prevent the intrusion of nonrelatives. Yet, there are exceptions an extreme case is the fusion of unrelated colonies. What are the advantages of fusions that have colonies with a high potential for conflict as a consequence? Here, we investigated fitness costs and benefits of colony fusions in a lower termite species, Cryptotermes secundus, in which more than 25% of all colonies in the field are fused. We found two benefits of colony fusion depending on colony size: very small colonies had an increased probability of survival when they fused, yet for most colony sizes mainly a few workers profit from colony fusions as their chance to become reproductives increased. This individual benefit was often costly for other colony members: colony growth was reduced and the current reproductives had an increased chance of dying when fusions were aggressive. Our study suggests that fusion of colonies often is the result of ‘selfish’ worker interests to become reproductives, and this might have been important for the termites' social evolution. Our results uniquely shows that selfish interests among related colony members can lead to the formation of groups with increased potential for conflict among less related members.     

对蜜蜂性别决定和蜂王级型确立理论的新诠释

从全新视角概貌性解读蜜蜂Apis诸多生殖机制,依据的就是蜂王或产卵工蜂的卵子发生、性别决定假说、性位点研究以及蜂王级型确立机制。这种不同于单倍-二倍性性别决定机制的新诠释,适用于明确性别决定机制、简化定向育种方法、减少比较性实验的难度和时间、实施亲子鉴定和抽象并量化种群的概念。