Judith Korb

Molecular traces of alternative social organization in a termite genome

Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.

Thermoregulation and ventilation of termite mounds.

Some of the most sophisticated of all animal-built structures are the mounds of African termites of the subfamily Macrotermitinae, the fungus-growing termites. They have long been studied as fascinating textbook examples of thermoregulation or ventilation of animal buildings. However, little research has been designed to provide critical tests of these paradigms, derived from a very small number of original papers. Here I review results from recent studies on Macrotermes bellicosus that considered the interdependence of ambient temperature, thermoregulation, ventilation and mound architecture, and that question some of the fundamental paradigms of termite mounds. M. bellicosus achieves thermal homeostasis within the mound, but ambient temperature has an influence too. In colonies in comparably cool habitats, mound architecture is adapted to reduce the loss of metabolically produced heat to the environment. While this has no negative consequences in small colonies, it produces a trade-off with gas exchange in large colonies, resulting in suboptimally low nest temperatures and increased CO2 concentrations. Along with the alteration in mound architecture, the gas exchange/ventilation mechanism also changes. While mounds in the thermally appropriate savannah have a very efficient circular ventilation during the day, the ventilation in the cooler forest is a less efficient upward movement of air, with gas exchange restricted by reduced surface exchange area. These results, together with other recent findings, question entrenched ideas such as the thermosiphon-ventilation mechanism or the assumption that mounds function to dissipate internally produced heat. Models trying to explain the proximate mechanisms of mound building, or building elements, are discussed.

Life history and development--a framework for understanding developmental plasticity in lower termites.

Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved complex societies independently and hence, their different ancestry provided them with different life‐history preadaptations for social evolution. Termites, the ‘social cockroaches’, have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non‐termitologists to access the literature.

Multilevel selection and social evolution of insect societies

How sterile, altruistic worker castes have evolved in social insects and how they are maintained have long been central topics in evolutionary biology. With the advance of kin selection theory, insect societies, in particular those of haplodiploid bees, ants, and wasps, have become highly suitable model systems for investigating the details of social evolution and recently also how within-group conflicts are resolved. Because insect societies typically do not consist of clones, conflicts among nestmates arise, for example about the partitioning of reproduction and the allocation of resources towards male and female sexuals. Variation in relatedness among group members therefore appears to have a profound influence on the social structure of groups. However, insect societies appear to be remarkably robust against such variation: division of labor and task allocation are often organized in more or less the same way in societies with high as in those with very low nestmate relatedness. To explain the discrepancy between predictions from kin structure and empirical data, it was suggested that constraints—such as the lack of power or information—prevent individuals from pursuing their own selfish interests. Applying a multilevel selection approach shows that these constraints are in fact group-level adaptation preventing or resolving intracolonial conflict. The mechanisms of conflict resolution in insect societies are similar to those at other levels in the biological hierarchy (e.g., in the genome or multicellular organisms): alignment of interests, fair lottery, and social control. Insect societies can thus be regarded as a level of selection with novelties that provide benefits beyond the scope of a solitary life. Therefore, relatedness is less important for the maintenance of insect societies, although it played a fundamental role in their evolution.

Complementary symbiont contributions to plant decomposition in a fungus-farming termite

Significance Old World (sub)tropical fungus-growing termites owe their massive ecological footprints to an advanced symbiosis with Termitomyces fungi. They also have abundant gut bacteria, but the complementarity roles of these symbionts have remained unclear. We analyzed the genomic potential for biomass decomposition in a farming termite, its fungal symbiont, and its bacterial gut communities. We found that plant biomass conversion is mostly a multistage complementary cooperation between Termitomyces and gut bacteria, with termite farmers primarily providing the gut compartments, foraging, and nest building. A mature queen had highly reduced gut microbial diversity for decomposition enzymes, suggesting she had an exclusively fungal diet even though she may have been the source of the gut microbes of the colony’s first workers and soldiers. Termites normally rely on gut symbionts to decompose organic matter but the Macrotermitinae domesticated Termitomyces fungi to produce their own food. This transition was accompanied by a shift in the composition of the gut microbiota, but the complementary roles of these bacteria in the symbiosis have remained enigmatic. We obtained high-quality annotated draft genomes of the termite Macrotermes natalensis, its Termitomyces symbiont, and gut metagenomes from workers, soldiers, and a queen. We show that members from 111 of the 128 known glycoside hydrolase families are represented in the symbiosis, that Termitomyces has the genomic capacity to handle complex carbohydrates, and that worker gut microbes primarily contribute enzymes for final digestion of oligosaccharides. This apparent division of labor is consistent with the Macrotermes gut microbes being most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and polysaccharide decomposition can proceed with high efficiency. Complex conversion of biomass in termite mounds thus appears to be mainly accomplished by complementary cooperation between a domesticated fungal monoculture and a specialized bacterial community. In sharp contrast, the gut microbiota of the queen had highly reduced plant decomposition potential, suggesting that mature reproductives digest fungal material provided by workers rather than plant substrate.

A Gene Necessary for Reproductive Suppression in Termites

Knocking out the Neofem2 gene in queen termites illicits pre-reproductive behavior in workers. A major transition in evolution is the origin of a division between reproduction and work among individuals. Nowhere is this divide more striking than in social insects, where workers rarely produce offspring even though they are often capable of reproduction should the queen or king die. The molecular mechanisms that control worker reproduction remain largely unknown. We used a combination of behavioral assays and RNA interference (RNAi) to identify a gene required for the reproductive division of labor between the queen and the workers.

Help or disperse? Cooperation in termites influenced by food conditions

Ecological factors have been claimed paramount for the evolution and maintenance of cooperative group living in eusocial termites, as well as in cooperatively breeding birds and mammals. However, a clear demonstration of the role of any specific ecological factor in termites has been lacking. In the termite Cryptotermes secundus, individuals have two options, staying as helpers at the natal nest or developing into winged sexuals that disperse to found new colonies. An important ecological factor expected to influence the course of termite development is food availability; C. secundus nests inside a single piece of wood that serves as the sole source of food for the duration of the colony. As wood is consumed, the longevity of the colony is reduced, thus diminishing the potential fitness gains of staying at the nest. We experimentally investigated the occurrence of cooperative behavior and development under abundant- and limited-food conditions. Workers exposed to food-limited conditions were more likely to develop into dispersing sexuals and increased “selfishly” their food-acquisition behaviors. Proximately, a reduced frequency of proctodeal trophallaxis may have interfered with the distribution of pheromones that inhibit sexual development. Ultimately, decreased inclusive fitness benefits in food-limited, and thus short-lived nests, appear to explain the development of dispersing sexuals, supporting (1) the benefits-of-philopatry hypothesis as developed for the occurrence of cooperative breeding in vertebrates, and (2) predictions of reproductive skew theories.

The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae)

Abstract. Mutualistic associations between different organisms are theoretically expected when the interests of independently reproducing units are aligned to form a single reproductive unit. This alignment does not come about easily, because models show that hosts and symbionts can be in conflict over the transmission of symbionts. Selection will favour hosts that are able to limit genetic variation of symbionts, for example by enforcing uniparental vertical transmission, while symbionts will be selected to disperse independently of the host. A crucial factor determining the evolution and elaboration of symbiotic relationships is therefore who controls the transmission of symbionts. In the fungus-growing termites (Macrotermintinae) horizontal transmission seems to be the rule as the termites normally acquire their cultivated fungus (Termitomyces) from the environment. In spite of this general pattern, uniparental, vertical transmission has evolved in two unrelated Macrotermitinae genera, where only one sex of the two primary reproductives carries asexual spores from the fungal comb of its parent colony to inoculate the new fungus comb. Remarkably, symbiont transmission is exclusively paternal in Macrotermes bellicosus, whereas symbionts are maternally inherited in all Microtermes species studied so far. Thus, in Macrotermitinae horizontal transmission is the ancestral state with two independent origins to uniparental, vertical transmission. This is in contrast to fungus-growing ants where uniparental, vertical transmission is the rule. Causes and consequences of this difference are further discussed. Despite this fundamental difference both groups evolved a similar symbiosis that is probably the key for their ecological success: the fungus-growing ants in the neotropics and the fungus-growing termites in the paleotropics.

Influence of environmental conditions on the expression of the sexual dispersal phenotype in a lower termite: implications for the evolution of workers in termites

Summary Phenotypic plasticity is thought to be of prime importance for the evolution of castes in social insects. However, conclusions are generally drawn from holometabolous social Hymenoptera, whereas little is known about the hemimetabolous termites. We investigated the influence of environmental conditions on the expression of the alternative phenotypes, worker versus dispersing sexual, in the drywood termite Cryptotermes secundus. Season played a fundamental role in this regulatory process by setting developmental deadlines. Individuals failing to reach these deadlines developed back to workers, whereas those in time progressed to dispersing sexuals. This seasonal regulation was superposed by the influence of food availability in the nest that adjusted the number of remaining workers versus dispersing sexuals. In line with declining benefits at the natal nest, there were more dispersing sexuals when the food was reduced. Provided that the life type of C. secundus reflects the ancestral state in termite evolution, as is often assumed, our results support the hypothesis that termite workers originated from individuals failing in sexual development. Furthermore, a taxonomical comparison between termite species with different life‐styles stresses the importance of a predictable variation in food availability for the existence of a plastic development and the occurrence of conditionally expressed phenotypes in termites. Compared with social Hymenoptera, the mechanisms involved in caste polyphenism in termites differed considerably, which demands more differentiated discussions about social insects caste polyphenism.

Molecular basis for the reproductive division of labour in a lower termite

BackgroundPolyphenism, the expression of different phenotypes with the same genetic background, is well known for social insects. The substantial physiological and morphological differences among the castes generally are the result of differential gene expression. In lower termites, workers are developmentally flexible to become neotenic replacement reproductives via a single moult after the death of the founding reproductives. Thus, both castes (neotenics and workers) are expected to differ mainly in the expression of genes linked to reproductive division of labour, which constitutes the fundamental basis of insect societies.ResultsRepresentational difference analysis of cDNAs was used to study differential gene expression between neotenics and workers in the drywood termite Cryptotermes secundus (Kalotermitidae). We identified and, at least partially cloned five novel genes that were highly expressed in female neotenics. Quantitative real-time PCR analysis of all five genes in different castes (neotenics, founding reproductives, winged sexuals and workers of both sexes) confirmed the differential expression patterns. In addition, the relative expression of these genes was determined in three body parts of female neotenics (head, thorax, and abdomen) using quantitative real-time PCR.ConclusionThe identified genes could be involved in the control and regulation of reproductive division of labour. Interestingly, this study revealed an expression pattern partly similar to social Hymenoptera indicating both common and species-specific regulatory mechanisms in hemimetabolous and holometabolous social insects.