Papers by Martin Kaltenpoth
The ISME journal, Jan 29, 2015
Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants r... more Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major force driving the diversification of phytophagous insects. Although symbiotic bacteria are known to have essential nutritional roles for insects, examples of radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts to diversify into the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria (Coriobacterium and Gordonibacter), as well as Firmicutes (Clostridium) and Proteobacteria (Klebsiella) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota...
Frontiers in Ecology and Evolution, 2014
Chemical communication in insects' sexual interactions is well-known to involve olfaction of vola... more Chemical communication in insects' sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.
Communicative & Integrative Biology, 2014
BMC microbiology, 2014
Background: 'Candidatus Streptomyces philanthi' is a monophyletic clade of formerly uncultured ba... more Background: 'Candidatus Streptomyces philanthi' is a monophyletic clade of formerly uncultured bacterial symbionts in solitary digger wasps of the genera Philanthus, Philanthinus and Trachypus (Hymenoptera, Crabronidae). These bacteria grow in female-specific antennal reservoirs andafter transmission to the cocoonproduce antibiotics protecting the host larvae from fungal infection. However, the symbionts' refractoriness to cultivation has thus far hampered detailed in vitro studies on their physiology and on the evolutionary changes in metabolic versatility in response to the host environment. Results: Here we isolated in axenic culture 22 'Streptomyces philanthi' biovars from different host species. Sequencing of gyrB revealed no heterogeneity among isolates within host individuals, suggesting low levels of (micro)diversity or even clonality of the symbionts in individual beewolf antennae. Surprisingly, however, isolates from different host species differed strongly in their physiology. All biovars from the Eurasian/African Philanthus and the South American Trachypus host species had high nutritional demands and were susceptible to most antibiotics tested, suggesting a tight association with the hosts. By contrast, biovars isolated from the genus Philanthinus and the monophyletic North American Philanthus clade were metabolically versatile and showed broad antibiotic resistance. Concordantly, recent horizontal symbiont transfer eventsreflected in different symbiont strains infecting the same host specieshave been described only among North American Philanthus species, altogether indicative of facultative symbionts potentially capable of a free-living lifestyle. Phylogenetic analyses reveal a strong correlation between symbiont metabolic versatility and host phylogeny, suggesting that the host environment differentially affects the symbionts' evolutionary fate. Although opportunistic bacteria were occasionally isolated from the antennae of different host species, only filamentous Actinobacteria (genera Streptomyces, Amycolatopsis and Nocardia) could replace 'S. philanthi' in the antennal gland reservoirs. Conclusion: Our results indicate that closely related bacteria from a monophyletic clade of symbionts can experience very different evolutionary trajectories in response to the symbiotic lifestyle, which is reflected in different degrees of metabolic versatility and host-dependency. We propose that the host-provided environment could be an important factor in shaping the degenerative metabolic evolution in the symbionts and deciding whether they evolve into obligate symbionts or remain facultative and capable of a host-independent lifestyle.
Proceedings of the National Academy of Sciences of the United States of America, Jan 29, 2014
Many insects rely on symbiotic microbes for survival, growth, or reproduction. Over evolutionary ... more Many insects rely on symbiotic microbes for survival, growth, or reproduction. Over evolutionary timescales, the association with intracellular symbionts is stabilized by partner fidelity through strictly vertical symbiont transmission, resulting in congruent host and symbiont phylogenies. However, little is known about how symbioses with extracellular symbionts, representing the majority of insect-associated microorganisms, evolve and remain stable despite opportunities for horizontal exchange and de novo acquisition of symbionts from the environment. Here we demonstrate that host control over symbiont transmission (partner choice) reinforces partner fidelity between solitary wasps and antibiotic-producing bacteria and thereby stabilizes this Cretaceous-age defensive mutualism. Phylogenetic analyses show that three genera of beewolf wasps (Philanthus, Trachypus, and Philanthinus) cultivate a distinct clade of Streptomyces bacteria for protection against pathogenic fungi. The symbio...
Proceedings. Biological sciences / The Royal Society, Jan 7, 2014
Despite the demonstrated functional importance of gut microbes, our understanding of how animals ... more Despite the demonstrated functional importance of gut microbes, our understanding of how animals regulate their metabolism in response to nutritionally beneficial symbionts remains limited. Here, we elucidate the functional importance of the African cotton stainer's (Dysdercus fasciatus) association with two actinobacterial gut symbionts and subsequently examine the insect's transcriptional response following symbiont elimination. In line with bioassays demonstrating the symbionts' contribution towards host fitness through the supplementation of B vitamins, comparative transcriptomic analyses of genes involved in import and processing of B vitamins revealed an upregulation of gene expression in aposymbiotic (symbiont-free) compared with symbiotic individuals; an expression pattern that is indicative of B vitamin deficiency in animals. Normal expression levels of these genes, however, can be restored by either artificial supplementation of B vitamins into the insect's...
PloS one, 2014
The acquisition and vertical transmission of bacterial symbionts plays an important role in insec... more The acquisition and vertical transmission of bacterial symbionts plays an important role in insect evolution and ecology. However, the molecular mechanisms underlying the stable maintenance and control of mutualistic bacteria remain poorly understood. The cotton stainer Dysdercus fasciatus harbours the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. in its midgut. The symbionts supplement limiting B vitamins and thereby significantly contribute to the host's fitness. In this study, we experimentally disrupted the symbionts' vertical transmission route and performed comparative transcriptomic analyses of genes expressed in the gut of aposymbiotic (symbiont-free) and control individuals to study the host immune response in presence and absence of the mutualists. Annotation of assembled cDNA reads identified a considerable number of genes involved in the innate immune system, including different protein isoforms of several immune effector proteins (spec...
Molecular Ecology Notes, 2004
ABSTRACT
Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence ... more Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect-bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.
Mutualistic, commensalistic or parasitic interactions are unevenly distributed across the animals... more Mutualistic, commensalistic or parasitic interactions are unevenly distributed across the animals and plants: in certain taxa, such interspecific associations evolved more often than in others. Within the ants, associations between species of the genera Camponotus and Crematogaster evolved repeatedly and include trail-sharing associations, where two species share foraging trails, and parabioses, where two species share a nest without aggression. Camponotus and Crematogaster may possess life-history traits that favour the evolution of associations. To identify which traits are affected by the association, we investigated a neotropical parabiosis of Ca. femoratus and Cr. levior and compared it to a paleotropical parabiosis and a trail-sharing association. The two neotropical species showed altered cuticular hydrocarbon profiles compared to non-parabiotic species accompanied by low levels of interspecific aggression. Both species occurred in two chemically distinct types. Camponotus followed artificial trails of Crematogaster pheromones, but not vice versa. The above traits were also found in the paleotropical parabiosis, and the trail-following results match those of the trail-sharing association. In contrast to paleotropical parabioses, however, Camponotus was dominant, had a high foraging activity and often fought against Crematogaster over food resources. We suggest three potential preadaptations for parabiosis. First, Crematogaster uses molecules as trail pheromones, which can be perceived by Camponotus, too. Second, nests of Camponotus are an important benefit to Crematogaster and may create a selection pressure for the latter to tolerate Camponotus. Third, there are parallel, but unusual, shifts in cuticular hydrocarbon profiles between neotropics and paleotropics, and between Camponotus and Crematogaster.
Division of reproductive labor in insect societies is often based on worker self-restraint and bo... more Division of reproductive labor in insect societies is often based on worker self-restraint and both queen and worker policing. Workers of many hitherto studied wasps, bees and ants do not lay eggs in the presence of a queen. However, it is presently unclear how far these observations in a few select clades can be generalized. We investigated if and how queens maintain a reproductive monopoly in colonies of the elongate twig ant, Pseudomyrmex gracilis, a member of the previously unstudied ant subfamily Pseudomyrmecinae. Colonies are usually headed by a single, singly mated queen (monogyny, monandry). Workers therefore would be more closely related to males produced by other workers (r=0.375) than to the sons of queens (r= 0.25). Nevertheless, workers appear to refrain from laying male-destined eggs in the presence of the queen. In queenless conditions, workers form dominance hierarchies by antennal boxing, and only one or a few high-ranking individuals readily begin to lay eggs. When returned into a queenright colony, egg-laying workers are immediately bitten, stung and expelled or killed by other workers. While the composition of cuticular hydrocarbons clearly differed between castes, it less clearly reflected worker ovarian development. An association with worker ovarian development that would allow workers to monitor the reproductive status of nestmates could only be tentatively postulated for certain substances. Our study broadens our knowledge about reproductive conflict in social Hymenoptera and shows that worker sterility in the presence of a queen is more common in monogynous, monandrous ants than expected from relatedness alone.
The antennae of female European beewolves (Philanthus triangulum, Hymenoptera: Crabronidae) conta... more The antennae of female European beewolves (Philanthus triangulum, Hymenoptera: Crabronidae) contain unique gland reservoirs that are inhabited by the symbiotic bacterium 'Candidatus Streptomyces philanthi'. The reservoir content is secreted into the subterranean brood cells where it serves a dual function: (1) It provides the larvae with spatial information about the orientation of cocoon spinning, and (2) it supplies the larva with the symbiotic bacteria that are needed for the protection of the cocoon against pathogenic microorganisms. We analyzed the hydrocarbon composition of the antennal gland secretion (AGS) by solid phase micro-extraction-gas chromatography-mass spectrometry. We detected 28 substances, the majority of which were saturated and unsaturated hydrocarbons, with minor amounts of some branched alkanes, two ketones, and three unknown substances. There was a strong dimorphism in the chemical composition of the AGS among beewolf females. The two morphs had either (Z)-9-pentacosene (C 25 -type) or (Z)-9-heptacosene (C 27 -type) as the main component, and they differed significantly in the relative amounts of most of the other AGS substances. The hydrocarbon composition of the AGS is very similar to that of the postpharyngeal gland of female beewolves, suggesting that the hydrocarbons are universally used for different purposes and transported into the gland from the hemolymph. The putative function of the hydrocarbons in the AGS is discussed.
Actinobacteria engage in defensive symbioses with several insect taxa, but reports of nutritional... more Actinobacteria engage in defensive symbioses with several insect taxa, but reports of nutritional contributions to their hosts have been exceptionally rare. Cotton stainers (Dysdercus fasciatus) and red firebugs (Pyrrhocoris apterus) (both Hemiptera, Pyrrhocoridae) harbour the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. as well as Firmicutes (Clostridium sp. and Lactococcus sp.) and Proteobacteria (Klebsiella sp. and a Rickettsiales bacterium) in the M3 region of their midgut. We combined experimental manipulation with community-level analyses to elucidate the function of the gut symbionts in both pyrrhocorid species. Elimination of symbionts by egg-surface sterilization resulted in significantly higher mortality and reduced growth rates, indicating that the microbial community plays an important role for host nutrition. Fitness of symbiont-deprived bugs could be completely restored by re-infection with the original microbiota, while reciprocal cross-infections of microbial communities across both pyrrhocorid species only partially rescued fitness, demonstrating a high degree of host-symbiont specificity. Community-level analyses by quantitative PCRs targeting the dominant bacterial strains allowed us to link the observed fitness effects to the abundance of the two actinobacterial symbionts. The nutritional mutualism with Actinobacteria may have enabled pyrrhocorid bugs to exploit Malvales seeds as a food source and thereby possibly allowed them to occupy and diversify in this ecological niche.
Physiological Entomology - PHYSIOL ENTOMOL, 2010
ABSTRACT Several insect taxa have evolved symbioses with actinobacteria that protect the host or ... more ABSTRACT Several insect taxa have evolved symbioses with actinobacteria that protect the host or its nutritional resources against pathogens. Digger wasps of the genus Philanthus (‘beewolves’; Hymenoptera, Crabronidae) cultivate ‘Candidatus Streptomyces philanthi’ (Ca. S. philanthi) in specialized antennal glands and transfer them to subterranean brood cells, where the symbionts provide protection for the beewolf larva against pathogens by producing a cocktail of antibiotic substances. The present study investigates the occurrence of antennal symbionts in two species of the genus Trachypus, which is the closest relative to Philanthus. Cross sections of the antennae from females of both Trachypus denticollis and Trachypus boharti reveal bacteria-containing gland reservoirs that are morphologically very similar to those found in Philanthus spp. Polymerase chain reaction-based screens with specific primers, sequencing of the partial 16S rRNA gene, and fluorescence in situ hybridization confirm the presence of close relatives of ‘Ca. S. philanthi’ in T. denticollis and T. boharti. However, 16S rRNA sequence divergence between Trachypus spp. and Philanthus spp. symbionts is much higher for T. boharti than for T. denticollis, suggesting that horizontal transmission and/or de novo uptake of symbionts from the environment occurs occasionally. The results obtained indicate that the protective symbiosis with antennal actinobacteria is older and more widespread than previously recognized and occurs in at least two genera of digger wasps that comprise approximately 170 species.
Current Biology, 2005
Symbiotic associations between different organisms are of great importance for evolutionary and e... more Symbiotic associations between different organisms are of great importance for evolutionary and ecological processes [1–4]. Bacteria are particularly valuable symbiotic partners owing to their huge diversity of biochemical pathways that may open entirely new ecological niches for higher organisms [1–3]. Here, we report on a unique association between a new Streptomyces species and a solitary hunting wasp, the European beewolf
PLoS ONE, 2013
Microbes pose severe threats to animals as competitors or pathogens and strongly affect the evolu... more Microbes pose severe threats to animals as competitors or pathogens and strongly affect the evolution of life history traits like parental care. Females of the European beewolf Philanthus triangulum, a solitary digger wasp, provision their offspring with paralyzed honeybees and embalm them with the secretion from large postpharyngeal glands (PPG) that contain mainly unsaturated hydrocarbons. This coating changes the physico-chemical properties of the prey surface, causes a reduction of water condensation and retards growth of mold fungi. Here we examined the closely related South American genus Trachypus, which shows a life-history similar to Philanthus. We investigated whether Trachypus spp. also possess PPGs and embalm larval provisions. Using histological methods and 3D reconstructions we show that Trachypus boharti and T. elongatus possess PPGs that are similar to P. triangulum but somewhat smaller. The ultrastructure of the gland epithelium suggests that the gland content is at least partly sequestered from the hemolymph. Chemical analyses using gas chromatography / mass spectrometry revealed that both the cuticle and PPGs of Trachypus contain mainly unsaturated long-chain hydrocarbons. The gland of T. boharti additionally contains long-chain ketones. The hydrocarbons from the PPG of T. elongatus occurred on prey bees excavated from nests in the field but not on conspecific control bees. While the embalming only slightly elevated the amount of hydrocarbons on prey bees, the proportion of unsaturated hydrocarbons, which is crucial for the antifungal effect, was significantly increased. The Trachypus species under study possess PPGs that are very similar to the PPG of P. triangulum with regard to morphology, ultrastructure and chemistry. Moreover, we provide clear evidence that T. elongatus females embalm their prey, presumably as a means of prey preservation. The observed differences among Trachypus and Philanthus in gland size and prey embalming may have evolved in response to divergent ecological conditions.
PLoS ONE, 2012
Mitochondrial genes in animals are especially useful as molecular markers for the reconstruction ... more Mitochondrial genes in animals are especially useful as molecular markers for the reconstruction of phylogenies among closely related taxa, due to the generally high substitution rates. Several insect orders, notably Hymenoptera and Phthiraptera, show exceptionally high rates of mitochondrial molecular evolution, which has been attributed to the parasitic lifestyle of current or ancestral members of these taxa. Parasitism has been hypothesized to entail frequent population bottlenecks that increase rates of molecular evolution by reducing the efficiency of purifying selection. This effect should result in elevated substitution rates of both nuclear and mitochondrial genes, but to date no extensive comparative study has tested this hypothesis in insects. Here we report the mitochondrial genome of a crabronid wasp, the European beewolf (Philanthus triangulum, Hymenoptera, Crabronidae), and we use it to compare evolutionary rates among the four largest holometabolous insect orders (Coleoptera, Diptera, Hymenoptera, Lepidoptera) based on phylogenies reconstructed with whole mitochondrial genomes as well as four single-copy nuclear genes (18S rRNA, arginine kinase, wingless, phosphoenolpyruvate carboxykinase). The mt-genome of P. triangulum is 16,029 bp in size with a mean A+T content of 83.6%, and it encodes the 37 genes typically found in arthropod mt genomes (13 protein-coding, 22 tRNA, and two rRNA genes). Five translocations of tRNA genes were discovered relative to the putative ancestral genome arrangement in insects, and the unusual start codon TTG was predicted for cox2. Phylogenetic analyses revealed significantly longer branches leading to the apocritan Hymenoptera as well as the Orussoidea, to a lesser extent the Cephoidea, and, possibly, the Tenthredinoidea than any of the other holometabolous insect orders for all mitochondrial but none of the four nuclear genes tested. Thus, our results suggest that the ancestral parasitic lifestyle of Apocrita is unlikely to be the major cause for the elevated substitution rates observed in hymenopteran mitochondrial genomes.
New Phytologist, 2014
Mutualistic ants are commonly considered as an efficient indirect defence against herbivores. Nev... more Mutualistic ants are commonly considered as an efficient indirect defence against herbivores. Nevertheless, their indirect protective role against plant pathogens has been scarcely investigated.
Uploads
Papers by Martin Kaltenpoth