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.

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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.

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