RESUMEN

Small-scale farming of edible insects could help combat public health challenges such as protein energy malnutrition and anemia, but reliable low-cost feeds for insects are needed. In resource-limited contexts, where grains such as maize are prohibitively costly for use as insect feed, the feasibility of insect farming may depend on finding alternatives. Here, we explore the potential to modify plentiful maize crop residue with edible mushroom mycelium to generate a low-cost feed adjunct for the farmed two-spotted cricket, Gryllus bimaculatus. Mushroom farming, like insect agriculture, is versatile; it can yield nutritious food while increasing system circularity by utilizing lignocellulosic residues from row crops as inputs. Pleurotus ostreatus, is an edible basidiomycete capable of being cultivated on corn stover (Zea mays). Mushroom harvest results in abundant "spent" substrate, which we investigated as a candidate feed ingredient. We created six cricket feeds containing fermented Pleurotus substrate plus an unfermented control, measuring cricket mass, mortality, and maturation weekly to evaluate cricket growth performance impacts of both fungal fermentation duration and mushroom formation. Pasteurized corn stover was inoculated with P. ostreatus mycelium and fermented for 0, 2, 3, 4, or 8 weeks. Some 4 and 8-week substrates were induced to produce mushrooms through manipulations of temperature, humidity, and light conditions. Dried fermented stover (40%) was added to a 1:1 corn/soy grain mix and fed to crickets ad libitum for 44 days. The unfermented control group showed higher survivorship compared to several fermented diets. Control group mass yield was higher for 2 out of 6 fermented diets. Little variation in cricket iron content was observed via ICP-spectrometry across feeds, averaging 2.46 mg/100 g. To determine bioavailability, we conducted in vitro Caco-2 human colon epithelial cell absorption assays, showing that iron in crickets fed fruiting-induced substrates was more bioavailable than in unfruited groups. Despite more bioavailable iron in crickets reared on post-fruiting substrates, we conclude that Pleurotus-fermented stover is an unsuitable feed ingredient for G. bimaculatus due to high mortality, variability in growth responses within treatments, and low mass yield.

RESUMEN

Some fungus-farming ambrosia beetles rely on multiple nutritional cultivars (Ascomycota: Ophiostomatales and/or yeasts) that seem to change in relative abundance over time. The succession of these fungi could benefit beetle hosts by optimal consumption of the substrate and extended longevity of the nest. However, abundances of fungal cultivars and other symbionts are poorly known and their culture-independent quantification over development has been studied in only a single species. Here, for the first time, we compared the diversity and succession of both fungal and bacterial communities of fungus gardens in the fruit-tree pinhole borer, Xyleborinus saxesenii, from field and laboratory nests over time. By amplicon sequencing of probed fungus gardens of both nest types at three development phases we showed an extreme reduction of diversity in both bacterial and fungal symbionts in laboratory nests. Furthermore, we observed a general transition from nutritional to non-beneficial fungal symbionts during beetle development. While one known nutritional mutualist, Raffaelea canadensis, was occurring more or less stable over time, the second mutualist R. sulphurea was dominating young nests and decreased in abundance at the expense of other secondary fungi. The quicker the succession proceeded, the slower offspring beetles developed, suggesting a negative role of these secondary symbionts. Finally, we found signs of transgenerational costs of late dispersal for daughters, possibly as early dispersers transmitted and started their own nests with less of the non-beneficial taxa. Future studies should focus on the functional roles of the few bacterial taxa that were present in both field and laboratory nests.

RESUMEN

Outside humans, true agriculture was previously thought to be restricted to social insects farming fungus. However, obligate farming of plants by ants was recently discovered in Fiji, prompting a re-examination of plant cultivation by ants. Here, we generate a database of plant cultivation by ants, identify three main types, and show that these interactions evolved primarily for shelter rather than food. We find that plant cultivation evolved at least 65 times independently for crops (~200 plant species), and 15 times in farmer lineages (~37 ant taxa) in the Neotropics and Asia/Australasia. Because of their high evolutionary replication, and variation in partner dependence, these systems are powerful models to unveil the steps in the evolution and ecology of insect agriculture.

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RESUMEN

Fungal cultivation is a defining feature for advanced agriculture in fungus-farming ants and termites. In a third supposedly fungus-farming group, wood-colonizing ambrosia beetles, an experimental proof for the effectiveness of beetle activity for selective promotion of their food fungi over others is lacking and farming has only been assumed based on observations of social and hygienic behaviours. Here, we experimentally removed mothers and their offspring from young nests of the fruit-tree pinhole borer, Xyleborinus saxesenii. By amplicon sequencing of bacterial and fungal communities of nests with and without beetles we could show that beetles are indeed able to actively shift symbiont communities. Although being consumed, the Raffaelea food fungi were more abundant when beetles were present while a weed fungus (Chaetomium sp.) as well as overall bacterial diversity were reduced in comparison to nests without beetles. Core symbiont communities were generally of low diversity and there were strong signs for vertical transmission not only for the cultivars, but also for secondary symbionts. Our findings verify the existence of active farming, even though the exact mechanisms underlying the selective promotion and/or suppression of symbionts need further investigation.

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Social animals are among the most successful organisms on the planet and derive many benefits from living in groups, including facilitating the evolution of agriculture. However, living in groups increases the risk of disease transmission in social animals themselves and the cultivated crops upon which they obligately depend. Social insects offer an interesting model to compare to human societies, in terms of how insects manage disease within their societies and with their agricultural symbionts. As living in large groups can help the spread of beneficial microbes as well as pathogens, we examine the role of defensive microbial symbionts in protecting the host from pathogens. We further explore how beneficial microbes may influence other pathogen defenses including behavioral and immune responses, and how we can use insect systems as models to inform on issues relating to human health and agriculture.

RESUMEN

Diverse forms of cultivation have evolved across the tree of life. Efficient farming requires that the farmer deciphers and actively promotes conditions that increase crop yield. For plant cultivation, this can include evaluating tradeoffs among light, nutrients, and protection against herbivores. It is not understood if, or how, nonhuman farmers evaluate local conditions to increase payoffs. Here, we address this question using an obligate farming mutualism between the ant Philidris nagasau and epiphytic plants in the genus Squamellaria that are cultivated for their nesting sites and floral rewards. We focused on the ants' active fertilization of their crops and their protection against herbivory. We found that ants benefited from cultivating plants in full sun, receiving 7.5-fold more floral food rewards compared to shade-cultivated plants. The higher reward levels correlated with higher levels of crop protection provided by the ants. However, while high-light planting yielded the greatest immediate food rewards, sun-grown crops contained less nitrogen compared to shade-grown crops. This was due to lower nitrogen input from ants feeding on floral rewards instead of insect protein gained from predation. Despite this tradeoff, farming ants optimize crop yield by selectively planting their crops in full sun. Ancestral state reconstructions across this ant-plant clade show that a full-sun farming strategy has existed for millions of years, suggesting that nonhuman farmers have evolved the means to evaluate and balance conflicting crop needs to their own benefit.

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RESUMEN

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.

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RESUMEN

Bark and ambrosia beetles are highly specialized weevils (Curculionidae) that have established diverse symbioses with fungi, most often from the order Ophiostomatales (Ascomycota, Sordariomycetes). The two types of beetles are distinguished by their feeding habits and intimacy of interactions with their symbiotic fungi. The tree tissue diet of bark beetles is facilitated by fungi, while ambrosia beetles feed solely on fungi that they farm. The farming life history strategy requires domestication of a fungus, which the beetles consume as their sole food source. Ambrosia beetles in the subfamily Platypodinae originated in the mid-Cretaceous (119-88 Ma) and are the oldest known group of farming insects. However, attempts to resolve phylogenetic relationships and the timing of domestication events for fungal cultivars have been largely inconclusive. We sequenced the genomes of 12 ambrosia beetle fungal cultivars and bark beetle associates, including the devastating laurel wilt pathogen, Raffaelea lauricola, to estimate a robust phylogeny of the Ophiostomatales. We find evidence for contemporaneous diversification of the beetles and their associated fungi, followed by three independent domestication events of the ambrosia fungi genus Raffaelea. We estimate the first domestication of an Ophiostomatales fungus occurred ~86 Ma, 25 million years earlier than prior estimates and in close agreement with the estimated age of farming in the Platypodinae (96 Ma). Comparisons of the timing of fungal domestication events with the timing of beetle radiations support the hypothesis that the first large beetle radiations may have spread domesticated "ambrosia" fungi to other fungi-associated beetle groups, perhaps facilitating the evolution of new farming lineages.

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