Many organisms team up with microbes for defense against predators, parasites, parasitoids, or pathogens. Here we review the described protective symbioses between animals (including marine invertebrates, nematodes, insects, and vertebrates) and bacteria, fungi, and dinoflagellates. We focus on associations where the microbial natural products mediating the protective activity have been elucidated or at least strong evidence for the role of symbiotic microbes in defense is available. In addition to providing an overview of the known defensive animal-microbe symbioses, we aim to derive general patterns on the chemistry, ecology, and evolution of such associations.
Division of labor among the workers of insect societies is a conspicuous feature of their biology. Social tasks are commonly shared among age groups but not between larvae and adults with completely different morphologies, as in bees, wasps, ants, and beetles (i.e., Holometabola). A unique yet hardly studied holometabolous group of insects is the ambrosia beetles. Along with one tribe of ants and one subfamily of termites, wood-dwelling ambrosia beetles are the only insect lineage culturing fungi, a trait predicted to favor cooperation and division of labor. Their sociality has not been fully demonstrated, because behavioral observations have been missing. Here we present behavioral data and experiments from within nests of an ambrosia beetle, Xyleborinus saxesenii. Larval and adult offspring of a single foundress cooperate in brood care, gallery maintenance, and fungus gardening, showing a clear division of labor between larval and adult colony members. Larvae enlarge the gallery and participate in brood care and gallery hygiene. The cooperative effort of adult females in the colony and the timing of their dispersal depend on the number of sibling recipients (larvae and pupae), on the presence of the mother, and on the number of adult workers. This suggests that altruistic help is triggered by demands of brood dependent on care. Thus, ambrosia beetles are not only highly social but also show a special form of division of labor that is unique among holometabolous insects.altruism | cooperative fungiculture | insect agriculture | larval workers | mutualism
The evolution of a mutualism requires reciprocal interactions whereby one species provides a service that the other species cannot perform or performs less efficiently. Services exchanged in insect–fungus mutualisms include nutrition, protection, and dispersal. In ectosymbioses, which are the focus of this review, fungi can be consumed by insects or can degrade plant polymers or defensive compounds, thereby making a substrate available to insects. They can also protect against environmental factors and produce compounds antagonistic to microbial competitors. Insects disperse fungi and can also provide fungal growth substrates and protection. Insect–fungus mutualisms can transition from facultative to obligate, whereby each partner is no longer viable on its own. Obligate dependency has ( a) resulted in the evolution of morphological adaptations in insects and fungi, ( b) driven the evolution of social behaviors in some groups of insects, and ( c) led to the loss of sexuality in some fungal mutualists.
Fungus cultivation by ambrosia beetles is one of the four independently evolved cases of agriculture known in animals. Such cultivation is most advanced in the highly social subtribe Xyleborina (Scolytinae), which is characterized by haplodiploidy and extreme levels of inbreeding. Despite their ubiquity in forests worldwide, the behavior of these beetles remains poorly understood. This may be in part because of their cryptic life habits within the wood of trees. Here we present data obtained by varying a laboratory breeding technique based on artificial medium inside glass tubes, which enables behavioral observations. We studied species of the three most widespread genera of Xyleborina in the temperate zone: Xyleborus, Xyleborinus, and Xylosandrus. We raised several generations of each species with good breeding success in two types of media. The proportion of females of Xyleborinus saxesenii Ratzeburg producing offspring within 40 d depended significantly on founder female origin, which shows a transgenerational effect. Labor-intensive microbial sterilization techniques did not increase females' breeding success relative to a group of females shortly treated with ethanol. Gallery productivity measured as the mean number of mature offspring produced after 40 d varied between species and was weakly affected by the type of medium used and foundress origin (field or laboratory) in X. saxesenii, whereas different preparation and sterilization techniques of the beetles had no effect. Behavioral observations showed the time course of different reproductive stages and enabled to obtain detailed behavioral information in all species studied. We propose that the laboratory techniques we describe here are suited for extensive studies of sociality and modes of agriculture in the xyleborine ambrosia beetles, which may yield important insights into the evolution of fungal agriculture and advanced social organization.
The genus Ambrosiella accommodates species of Ceratocystidaceae (Microascales) that are obligate, mutualistic symbionts of ambrosia beetles, but the genus appears to be polyphyletic and more diverse than previously recognized. In addition to Ambrosiella xylebori, Ambrosiella hartigii, Ambrosiella beaveri, and Ambrosiella roeperi, three new species of Ambrosiella are described from the ambrosia beetle tribe Xyleborini: Ambrosiella nakashimae sp. nov. from Xylosandrus amputatus, Ambrosiella batrae sp. nov. from Anisandrus sayi, and Ambrosiella grosmanniae sp. nov. from Xylosandrus germanus. The genus Meredithiella gen. nov. is created for symbionts of the tribe Corthylini, based on Meredithiella norrisii sp. nov. from Corthylus punctatissimus. The genus Phialophoropsis is resurrected to accommodate associates of the Xyloterini, including Phialophoropsis trypodendri from Trypodendron scabricollis and Phialophoropsis ferruginea comb. nov. from Trypodendron lineatum. Each of the ten named species was distinguished by ITS rDNA barcoding and morphology, and the ITS rDNA sequences of four other putative species were obtained with Ceratocystidaceae-specific primers and template DNA extracted from beetles or galleries. These results support the hypothesis that each ambrosia beetle species with large, complex mycangia carries its own fungal symbiont. Conidiophore morphology and phylogenetic analyses using 18S (SSU) rDNA and TEF1α DNA sequences suggest that these three fungal genera within the Ceratocystidaceae independently adapted to symbiosis with the three respective beetle tribes. In turn, the beetle genera with large, complex mycangia appear to have evolved from other genera in their respective tribes that have smaller, less selective mycangia and are associated with Raffaelea spp. (Ophiostomatales).
SignificanceAmbrosia beetles are among the true fungus-farming insects and cultivate fungal gardens on which the larvae and adults feed. After invading new habitats, some species destructively attack living or weakened trees growing in managed and unmanaged settings. Ambrosia beetles adapted to weakened trees tunnel into stem tissues containing ethanol to farm their symbiotic fungi, even though ethanol is a potent antimicrobial agent that inhibits the growth of various fungi, yeasts, and bacteria. Here we demonstrate that ambrosia beetles rely on ethanol for host tree colonization because it promotes the growth of their fungal gardens while inhibiting the growth of “weedy” fungal competitors. We propose that ambrosia beetles use ethanol to optimize their food production.
The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also independently evolved symbioses with fungi that they cultivate for food. Despite occurring across divergent insect and fungal lineages, the fungivorous niches of these insects are remarkably similar, indicating convergent evolution toward this successful ecological strategy. Here, we characterize the microbiota of ants, beetles, and termites engaged in nutritional symbioses with fungi to define the bacterial groups associated with these prominent herbivores and forest pests. Using culture-independent techniques and the in silico reconstruction of 37 composite genomes of dominant community members, we demonstrate that different insect-fungal symbioses that collectively shape ecosystems worldwide have highly similar bacterial microbiotas comprised primarily of the genera Enterobacter, Rahnella, and Pseudomonas. Although these symbioses span three orders of insects and two phyla of fungi, we show that they are associated with bacteria sharing high whole-genome nucleotide identity. Due to the fine-scale correspondence of the bacterial microbiotas of insects engaged in fungal symbioses, our findings indicate that this represents an example of convergence of entire host-microbe complexes.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.