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Featured researches published by Duur K. Aanen.


Proceedings of the National Academy of Sciences of the United States of America | 2002

The evolution of fungus-growing termites and their mutualistic fungal symbionts

Duur K. Aanen; Paul Eggleton; Corinne Rouland-Lefèvre; Tobias Guldberg-Frøslev; Søren Rosendahl; Jacobus J. Boomsma

We have estimated phylogenies of fungus-growing termites and their associated mutualistic fungi of the genus Termitomyces using Bayesian analyses of DNA sequences. Our study shows that the symbiosis has a single African origin and that secondary domestication of other fungi or reversal of mutualistic fungi to a free-living state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite species can have different symbionts. Data are consistent with horizontal transmission of fungal symbionts in both the ancestral state of the mutualism and most of the extant taxa. Clonal vertical transmission of fungi, previously shown to be common in the genus Microtermes (via females) and in the species Macrotermes bellicosus (via males) [Johnson, R. A., Thomas, R. J., Wood, T. G. & Swift, M. J. (1981) J. Nat. Hist. 15, 751–756], is derived with two independent origins. Despite repeated host switching, statistical tests taking phylogenetic uncertainty into account show a significant congruence between the termite and fungal phylogenies, because mutualistic interactions at higher taxonomic levels show considerable specificity. We identify common characteristics of fungus-farming evolution in termites and ants, which apply despite the major differences between these two insect agricultural systems. We hypothesize that biparental colony founding may have constrained the evolution of vertical symbiont transmission in termites but not in ants where males die after mating.


PLOS Genetics | 2014

Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus

Kui Lin; Erik Limpens; Zhonghua Zhang; Sergey Ivanov; Diane G. O. Saunders; Desheng Mu; Erli Pang; Huifen Cao; Hwangho Cha; Tao Lin; Qian Zhou; Yi Shang; Ying Li; Trupti Sharma; Robin van Velzen; Norbert C.A. de Ruijter; Duur K. Aanen; Joe Win; Sophien Kamoun; Ton Bisseling; René Geurts; Sanwen Huang

Nuclei of arbuscular endomycorrhizal fungi have been described as highly diverse due to their asexual nature and absence of a single cell stage with only one nucleus. This has raised fundamental questions concerning speciation, selection and transmission of the genetic make-up to next generations. Although this concept has become textbook knowledge, it is only based on studying a few loci, including 45S rDNA. To provide a more comprehensive insight into the genetic makeup of arbuscular endomycorrhizal fungi, we applied de novo genome sequencing of individual nuclei of Rhizophagus irregularis. This revealed a surprisingly low level of polymorphism between nuclei. In contrast, within a nucleus, the 45S rDNA repeat unit turned out to be highly diverged. This finding demystifies a long-lasting hypothesis on the complex genetic makeup of arbuscular endomycorrhizal fungi. Subsequent genome assembly resulted in the first draft reference genome sequence of an arbuscular endomycorrhizal fungus. Its length is 141 Mbps, representing over 27,000 protein-coding gene models. We used the genomic sequence to reinvestigate the phylogenetic relationships of Rhizophagus irregularis with other fungal phyla. This unambiguously demonstrated that Glomeromycota are more closely related to Mucoromycotina than to its postulated sister Dikarya.


Science | 2009

High Symbiont Relatedness Stabilizes Mutualistic Cooperation in Fungus-Growing Termites

Duur K. Aanen; Henrik H. De Fine Licht; Alfons J. M. Debets; Niels A. G. Kerstes; Rolf F. Hoekstra; Jacobus J. Boomsma

Gardening for Ants and Termites Among the social insects, ants and termites are the most diverse and ecologically dominant. Termites are known to engage in a mutualism with nitrogen-fixing bacteria, and Pinto-Tomás et al. (p. 1120) have identified similar relationships occurring among leaf-cutter ants, which maintain specialized nitrogen-fixing bacteria in their fungus gardens. Together, these mutualisms are a major source of nitrogen in terrestrial ecosystems. How is the evolutionary stability of such mutualistic cooperation maintained? Aanen et al. (p. 1103) show that the Termitomyces fungus cultured by termites remains highly related because mycelia of the same clone fuse together and grow more efficiently to out-compete rare clones. In symbioses of independently reproducing partners, a genetically uniform population of symbionts excludes cheating variants. It is unclear how mutualistic relationships can be stable when partners disperse freely and have the possibility of forming associations with many alternative genotypes. Theory predicts that high symbiont relatedness should resolve this problem, but the mechanisms to enforce this have rarely been studied. We show that African fungus-growing termites propagate single variants of their Termitomyces symbiont, despite initiating cultures from genetically variable spores from the habitat. High inoculation density in the substrate followed by fusion among clonally related mycelia enhances the efficiency of spore production in proportion to strain frequency. This positive reinforcement results in an exclusive lifetime association of each host colony with a single fungal symbiont and hinders the evolution of cheating. Our findings explain why vertical symbiont transmission in fungus-growing termites is rare and evolutionarily derived.


Insectes Sociaux | 2004

The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule

Seirian Sumner; Duur K. Aanen; J. H. C. Delabie; Jacobus J. Boomsma

SummaryEmery’s rule predicts that social parasites and their hosts share common ancestry and are therefore likely to be close relatives. Within the leaf-cutting ant genus Acromyrmex, two taxa of social parasites have been found, which are thought to occupy opposite grades of permanent social parasitism, based on their contrasting morphologies: Acromyrmex insinuator differs little in morphology from its free-living congeneric host species and produces a worker caste, and is thus thought to represent an early grade of social parasitism. At the other extreme, Pseudoatta spp. exhibit a very specialised morphology and lack a worker caste, both of which are characteristics of an evolutionarily derived grade of social parasitism. Here we present a molecular phylogeny using partial sequences of cytochrome oxidase I and II of about half of the known Acromyrmex species including two social parasites, their hosts and all congeneric species occurring sympatrically. We show that the two inquiline parasites represent two separate origins of social parasitism in the genus Acromyrmex. The early-grade social parasite A. insinuator is highly likely to be the sister species of its host Acromyrmex echinator, but the derived social parasite Pseudoatta sp. is not the sister species of its extant host Acromyrmex rugosus.


Proceedings of the National Academy of Sciences of the United States of America | 2014

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

Michael Poulsen; Haofu Hu; Cai Li; Zhensheng Chen; Luohao Xu; Saria Otani; Sanne Nygaard; Tania Nobre; Sylvia Klaubauf; Philipp M. Schindler; Hailin Pan; Zhikai Yang; A.S.M. Sonnenberg; Z. Wilhelm; Yong Zhang; Michael J. Wingfield; Cornelis J. P. Grimmelikhuijzen; Judith Korb; Duur K. Aanen; Jun Wang; Jacobus J. Boomsma; Guojie Zhang

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.


Molecular Ecology | 2014

Identifying the core microbial community in the gut of fungus-growing termites

Saria Otani; Aram Mikaelyan; Tânia Nobre; Lars Hestbjerg Hansen; Ngolo Abdoulaye Kone; Søren J. Sørensen; Duur K. Aanen; Jacobus J. Boomsma; Andreas Brune; Michael Poulsen

Gut microbes play a crucial role in decomposing lignocellulose to fuel termite societies, with protists in the lower termites and prokaryotes in the higher termites providing these services. However, a single basal subfamily of the higher termites, the Macrotermitinae, also domesticated a plant biomass‐degrading fungus (Termitomyces), and how this symbiont acquisition has affected the fungus‐growing termite gut microbiota has remained unclear. The objective of our study was to compare the intestinal bacterial communities of five genera (nine species) of fungus‐growing termites to establish whether or not an ancestral core microbiota has been maintained and characterizes extant lineages. Using 454‐pyrosequencing of the 16S rRNA gene, we show that gut communities have representatives of 26 bacterial phyla and are dominated by Firmicutes, Bacteroidetes, Spirochaetes, Proteobacteria and Synergistetes. A set of 42 genus‐level taxa was present in all termite species and accounted for 56–68% of the species‐specific reads. Gut communities of termites from the same genus were more similar than distantly related species, suggesting that phylogenetic ancestry matters, possibly in connection with specific termite genus‐level ecological niches. Finally, we show that gut communities of fungus‐growing termites are similar to cockroaches, both at the bacterial phylum level and in a comparison of the core Macrotermitinae taxa abundances with representative cockroach, lower termite and higher nonfungus‐growing termites. These results suggest that the obligate association with Termitomyces has forced the bacterial gut communities of the fungus‐growing termites towards a relatively uniform composition with higher similarity to their omnivorous relatives than to more closely related termites.


Mycologia | 2000

Phylogenetic relationships in the genus Hebeloma based on ITS1 and 2 sequences, with special emphasis on the Hebeloma crustuliniforme complex

Duur K. Aanen; Thomas W. Kuyper; Teun Boekhout; Rolf F. Hoekstra

Phylogenetic relationships within the ge- nus Hebeloma (Cortinariaceae, Agaricales) were de- termined, based on nuclear ribosomal ITS sequenc- es, using cladistic methods. Special emphasis was on phylogenetic relationships within the H. crustulini- forme complex. In total 52 sequences were analysed, representing 51 collections and 39 taxa. Agrocybe praecox and two species of Alnicola were used as out- groups. The genus Hebeloma appears to be mono- phyletic. Several well supported clades could be rec- ognized. However, many of the basal relationships are unresolved or only weakly supported. Alternative to- pologies could not be rejected. It is therefore impos- sible to derive a revised infrageneric classification of Hebeloma. The H. crustuliniforme complex appears paraphyletic, consisting of two clades with three and 17 intercompatibility groups respectively. In the sec- ond clade many of the phylogenetic relationships are also unresolved, reflecting a high rate of recent spe- ciation events. Most of the species in this clade form ectomycorrhizae with members of the Salicaceae. The taxon that is basal to this clade, however, is not associated with these hosts. The host tree switch to


Behavioral Ecology and Sociobiology | 2003

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

Judith Korb; Duur K. Aanen

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.


Fungal Biology | 2001

A widely distributed ITS polymorphism within a biological species of the ectomycorrhizal fungus Hebeloma velutipes

Duur K. Aanen; Thomas W. Kuyper; Rolf F. Hoekstra

The ectomycorrhizal fungus Hebeloma velutipes consists of two biological species (BSP 16 and 17). Within BSP 17 a dikaryon was found with two divergent types of the ribosomal Internal Transcribed Spacer (ITS1 and 2). The two ITS types segregated in monokaryotic progeny of that dikaryon, showing that these different ITS types represent different alleles at homologous rDNA loci in the two nuclei. RFLP analysis of a number of strains of BSP 17 showed that the polymorphism is widespread in Europe. There was no deficiency of the heterokaryotic type, demonstrating that ITS divergence in this species is not correlated with reduced intercompatibility. A strain from North America, not assigned to a biological species, showed the same polymorphism. Cladistic analysis of the two ITS sequences showed that they were not sister groups. One of the ITS types formed a monophyletic group together with the ITS type of BSP 16, the other type formed a clade with the ITS type of H. incarnatulum (BSP 18). BSP 16 and 17 showed partial intercompatibility. However, several lines of evidence suggest that the polymorphism of BSP 17 is not the result of frequent and continuing hybridisation with BSP 16. Instead, we give arguments for the hypothesis that the polymorphism evolved in allopatry and that the two types have come together relatively recently. The results of the polymorphism indicate a potential problem for molecular identification of fungal species based on ITS fingerprinting. The results also show that no generalisations are possible about the relation of speciation (the formation of BSP) and nuclear ITS divergence.


Philosophical Transactions of the Royal Society B | 2014

The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance?

Madeleine Beekman; Damian K. Dowling; Duur K. Aanen

Eukaryotic cells typically contain numerous mitochondria, each with multiple copies of their own genome, the mtDNA. Uniparental transmission of mitochondria, usually via the mother, prevents the mixing of mtDNA from different individuals. While on the one hand, this should resolve the potential for selection for fast-replicating mtDNA variants that reduce organismal fitness, maternal inheritance will, in theory, come with another set of problems that are specifically relevant to males. Maternal inheritance implies that the mitochondrial genome is never transmitted through males, and thus selection can target only the mtDNA sequence when carried by females. A consequence is that mtDNA mutations that confer male-biased phenotypic expression will be prone to evade selection, and accumulate. Here, we review the evidence from the ecological, evolutionary and medical literature for male specificity of mtDNA mutations affecting fertility, health and ageing. While such effects have been discovered experimentally in the laboratory, their relevance to natural populations—including the human population—remains unclear. We suggest that the existence of male expression-biased mtDNA mutations is likely to be a broad phenomenon, but that these mutations remain cryptic owing to the presence of counter-adapted nuclear compensatory modifier mutations, which offset their deleterious effects.

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Alfons J. M. Debets

Wageningen University and Research Centre

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Rolf F. Hoekstra

Wageningen University and Research Centre

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Tânia Nobre

Wageningen University and Research Centre

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Thomas W. Kuyper

Wageningen University and Research Centre

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Saria Otani

University of Copenhagen

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Tania Nobre

Wageningen University and Research Centre

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Corinne Rouland-Lefèvre

Institut de recherche pour le développement

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