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Korb, J.

Publications and source records attributed to Korb, J..

9 recordsLinked to original sources

Tracking a major evolutionary transition to superorganismality

Major transitions in evolution are associated with the loss of independent reproduction by formerly autonomous units. Termites provide a powerful system for studying this process because they exhibit diverse social systems in which worker developmental and reproductive potential declines with increasing colony-level organismality. However, the evolutionary sequence and developmental genetic basis of these transitions remain unresolved. Here, using comparative developmental transcriptomics across seven termite species that differ in workers' reproductive potential, we reconstructed the evolutionary history of termite social systems. We found that linear caste development, in which workers retain full reproductive potential, represents the ancestral state of termites. Bifurcated caste development, in which workers partially lose reproductive potential early in development, evolved independently multiple times, with two origins subsequently giving rise to superorganisms with unipotent, sterile workers. Ancestral gene regulatory network (GRN) reconstruction revealed that linear caste development evolved through retention of a juvenile-like worker state and co-option of a conserved developmental GRN characterizing hemimetabolous insect nymphal development, in which juvenile hormone, ecdysone and TGF-{beta} signaling pathways play central roles. The convergent evolution of bifurcated caste development repeatedly co-opted the GRN underlying linear caste development, heterochronically shifting its activity to earlier developmental stages. Finally, we found that the evolution of termite superorganisms involved somatization of the worker caste and co-option of a conserved endocrine GRN for terminal differentiation. Together, these findings uncovered repeated routes to reduced workers' reproductive potential through GRN co-option and highlight striking parallels between superorganism evolution in social insects and organismal evolution in metazoans.

evolutionary biology↗

Unexpectedly low recombination rates and presence of hotspots in termite genomes

Meiotic recombination is a fundamental evolutionary process that facilitates adaptation and the removal of deleterious genetic variation. Social Hymenoptera exhibit some of the highest recombination rates among metazoans, whereas high recombination rates have not been found among non-social species from this insect order. It is unknown whether elevated recombination rates are a ubiquitous feature of all social insects. In many metazoan taxa, recombination is mainly restricted to hotspots a few kilobases in length. However, little is known about the prevalence of recombination hotspots in insect genomes. Here we infer recombination rate and its fine-scale variation across the genomes of two social species from the insect order Blattodea: the termites Macrotermes bellicosus and Cryptotermes secundus. We used linkage-disequilibrium-based methods to infer recombination rate. We infer that recombination rates are close to 1 cM/Mb in both species, similar to the average metazoan rate. We also observed a highly punctate distribution of recombination in both termite genomes, indicative of the presence of recombination hotspots. We infer the presence of full-length PRDM9 genes in the genomes of both species, which suggests recombination hotspots in termites might be determined by PRDM9, as they are in mammals. We also find that recombination rates in genes are correlated with inferred levels of germline DNA methylation. The finding of low recombination rates in termites indicates that eusociality is not universally connected to elevated recombination rate. We speculate that the elevated recombination rates in social Hymenoptera are instead promoted by intense selection among haploid males.

genomics↗

High-quality long-read genome assemblies reveal evolutionary patterns of transposable elements and DNA methylation in termites

Arms races between parasites and hosts are key drivers of evolution. Selfishly replicating transposable elements (TEs) are thought to follow similar dynamics, but strong evidence is missing. We tested this in termites, social insects in which TEs have been linked to ageing. Sequencing genomes and profiling DNA methylation across the termite phylogeny revealed corresponding phylogenetic signals in TEs and TE methylation, indicative of selection. TE methylation reduces TE success, as both TE abundance and spreading efficiency decrease with increasing methylation. TEs also become less harmful with TE age: evolutionarily older TEs spread less, insert less into exons, and erode into short remnants. Correspondingly, defence through methylation is strongest against young TEs. Yet, as in typical host-parasite arms races, some TEs persist, implying resistance or recurrent invasions. Our results reveal arms races between TEs and DNA methylation, positioning TEs as drivers of genome evolution similar to symbionts in organismic evolution.

evolutionary biology↗

Disentangling the aging network of a termite queen

BackgroundMost insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster. By contrast, the queens of social insects (termites, ants, some bees and wasps) can live for more than a decade. This makes social insects promising new models in aging research providing insights into how a long reproductive life can be achieved. Yet, aging studies on social insect reproductives are hampered by a lack of quantitative data on age-dependent survival and time series analyses that cover the whole lifespan of such long-lived individuals. We studied aging in queens of the drywood termite Cryptotermes secundus by determining survival probabilities over more than 15 years and performed transcriptome analyses for queens of known age that covered their whole lifespan. ResultsThe maximum lifespan of C. secundus queens was 13 years with a median maximum longevity of 11.0 years. Time course and co-expression network analyses of gene expression patterns over time indicated a non-gradual aging pattern. It was characterized by networks of genes that became differentially expressed only late in life, namely after an age of 10 years, which associates well with the median maximum lifespan for queens. These old-age gene networks reflect processes of physiological upheaval. We detected strong signs of stress, decline, defence and repair at the transcriptional level of epigenetic control as well as at the post-transcriptional level with changes in transposable element activity and the proteostasis network. The latter depicts an upregulation of protein degradation, together with protein synthesis and protein folding, processes which are often down-regulated in old animals. The simultaneous upregulation of protein synthesis and autophagy is indicative for a stress-response mediated by the transcription factor cnc, a homolog of human nrf genes. ConclusionOur results show non-linear senescence with a rather sudden physiological upheaval at old-age. Most importantly, they point to a re-wiring in the proteostatis network as central for explaining the long life of social insect queens.

evolutionary biology↗

No evidence for immune-gene specific signals of selection in termites

It has been hypothesized that selection pressure from pathogens plays an important role in shaping social evolution. Social behaviour, in particular brood care, is associated with pathogen pressure in wood-dwelling \"lower\" termites. Yet, generally pathogen pressure is low in wood-dwelling termite species that never leave the nest except for the mating flight. In comparison, pathogen pressure is higher in species that leave the nest to forage, and thus constantly encounter a diversity of microbes from their environment. We hypothesized that such differences in pathogen pressure are also reflected by differences in the intensity of natural selection on immune genes. We tested this hypothesis in a phylogenetic framework, analyzing rates of non-synonymous and synonymous substitutions on single-copy immune genes. Therefore, we leveraged recent genomic and transcriptomic data from eight termite species, representing wood-dwelling and foraging species as well as 14 additional species spanning the winged insects (Pterygota). Our results provide no evidence for a role of pathogen pressure in selection intensity on single-copy immune genes. Instead, we found evidence for a genome-wide pattern of relaxed selection in termites.\n\nLife Science Identifiers (as available Zoobank)Ephemera danica:\n\nurn:lsid:zoobank.org:act:06633F75-4809-4BB3-BDCB-6270795368D5\n\nCoptotermes sp.\n\nurn:lsid:zoobank.org:pub:D6724B7F-F27A-47DC-A4FC-12859ECA0C71\n\nBlattella germanica:\n\nrn:lsid:zoobank.org:pub:1EA126BA-E9D2-4AA6-8202-26BA5B09B8AD\n\nLocusta migratoria\n\nurn:lsid:zoobank.org:pub:D792A09E-844A-412A-BFCA-5293F8388F8C\n\nPeriplaneta americana (Blatta americana):\n\nurn:lsid:zoobank.org:act:95113A55-4C6D-4DC7-A0E5-620BACADFFE5\n\nApis mellifera:\n\nurn:lsid:zoobank.org:act:9082C709-6347-4768-A0DC-27DC44400CB2\n\nBombyx mori (Phalaena (Bombyx) mori)\n\nurn:lsid:zoobank.org:act:215466E3-E77F-46E9-8097-372837D7A375\n\nDrosophila melanogaster:\n\nurn:lsid:zoobank.org:act:5B39F0AA-270D-4AA8-B9A3-C36A3A265910

evolutionary biology↗

Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host

BackgroundElucidating the interplay between hosts and their microbiomes in ecological adaptation has become a central theme in evolutionary biology. A textbook example of microbiome-mediated adaptation is the adaptation of lower termites to a wood-based diet, as they depend on their gut microbiome to digest wood. Lower termites have further adapted to different life types. Termites of the wood-dwelling life type never leave their nests and feed on a uniform diet. Termites of the foraging life type forage for food outside the nest and have access to other nutrients. Here we sought to investigate whether the microbiome that is involved in food substrate breakdown and nutrient acquisition might contribute to adaptation to these ecological differences. We reasoned that this should leave ecological imprints on the microbiome.\n\nResultsWe investigated the protist and bacterial microbiomes of a total of 29 replicate colonies from five termite species, covering both life types, using metagenomic shotgun sequencing. The microbiome of wood-dwelling species with a uniform wood diet was enriched for genes involved in lignocellulose degradation. Furthermore, metagenomic patterns suggest that the microbiome of wood-dwelling species relied primarily on direct fixation of atmospheric nitrogen, while the microbiome of foraging species entailed the necessary pathways to utilize nitrogen in the form of nitrate for example from soil.\n\nConclusionOur findings are consistent with the notion that the microbiome of wood-dwelling species bears an imprint of its specialization on degrading a uniform wood diet, while the microbiome of the foraging species might reflect its adaption to access growth limiting nutrients from more diverse sources. This supports the idea that specific subsets of functions encoded by the microbiome can contribute to host adaptation.

evolutionary biology↗

Hemimetabolous genomes reveal molecular basis of termite eusociality

Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the first, 2GB genome of a cockroach, Blattella germanica, and the 1.3GB genome of the drywood termite, Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.

evolutionary biology↗

Termite communities along a disturbance gradient in a West African savanna

Termites are important ecosystem engineers, crucial for the maintenance of tropical biodiversity and ecosystem functioning. But they are also pests which cause billions of dollars in damage annually to humans. Currently, our understanding of the mechanisms influencing species occurrences is limited and we do not know what distinguishes pest from non-pest species. We analyzed how anthropogenic disturbance (agriculture) affects species occurrences. We tested the hypothesis that strong disturbance functions as a habitat filter and selects for a subset of species which are major pests of crop. Using a cross-sectional approach, we studied termite community composition along a disturbance gradient from fields to 12-year-old fallows in a West African savanna. We reliably identified 19 species using genetic markers with a mean of about 10 species - many of them from the same feeding type - co-occurring locally. Supporting our hypothesis, disturbance was associated with environmental filtering of termites from the regional species pool, maybe via its effect on vegetation type. The most heavily disturbed sites were characterized by a subset of termite species which are well-known pests of crop. This is in line with the idea that strong anthropogenic disturbance selects for termite pest species.

ecology↗

Bacterial but not protist gut microbiota align with ecological specialization in a set of lower termite species

The role of microbes in adaptation of higher organisms to the environment is becoming increasingly evident, but remains poorly understood. Protist and bacterial microbes facilitate that lower termites thrive on wood and are directly involved in substrate break down. During the course of evolution lower termites adapted to different diets and lifestyles. In order to test whether there are changes of the termite gut microbiota that co-occur and hence could be related to diet and lifestyle adaptation, we assessed the bacterial and protist communities in a multispecies framework profiling three wood-dwelling and two foraging lower termite species using 16S and 18S rRNA gene amplicon sequencing. Termites were kept under controlled conditions on the same diet to minimize environmental effects on their gut microbiota. We found that protist communities group according to host phylogeny while bacterial communities group according to lifestyle. The change from the ancestral wood-dwelling to a foraging lifestyle coincides with exposure to more diverse and higher concentrations of pathogens as well as a more diverse diet. Accordingly, we identified bacteria that are associated with foraging termites of the genus Reticulitermes and could function as probiotics or be metabolically important on a more diverse diet. Furthermore, protist and bacterial diversity are correlated, suggesting not only that many termite gut bacteria are associated with protists, but also suggesting a role of protist diversity in the evolution of bacterial diversity in the termite gut or vice versa.

evolutionary biology↗