Think of weevils and most likely you'll think of spoiled food. But some weevils have turned to farming...

Insect agriculture, in the form of fungus cultivation, is best known from the attine ants and termites. However, in terms of the number of evolutionary origins, these insects are easily outclassed by the beetles, where farming has independently evolved several times. Given it’s convergence, not surprisingly these three insect groups with behaviourally complex agriculture systems show multiple similarities, but beetles are generally less well studied than ants and termites.

Agriculture in ambrosia beetles

The best-known beetle fungiculturists are the so-called ambrosia beetles, a diverse group of derived weevils in the subfamilies Scolytinae and Platypodinae. These subfamilies contain about 7500 species, which have the unusual habit of burrowing inside trees for feeding and oviposition as adults. They carve out intricate tunnel systems referred to as galleries, and this lifestyle probably facilitated the diversification of mutual associations with fungi. There are about 3400 described species of ambrosia beetle, which are most diverse in the tropics, and fungus cultivation is most advanced in the Xyleborini (Scolytinae). This highly social subtribe comprises about 1300 species with variable life histories but very similar fungiculture.

Symbiotic association with fungi

Ambrosia beetles depend on so-called ambrosia fungi, which they “farm” inside galleries excavated in the xylem of trees.As the wood is typically dead or decaying, the beetles seldom do any economic damage (in contrast to the related bark beetles that can be serious pests, especially by introducing infections). The ambrosia fungi are ascomycetes in the order Ophiostomatales (e.g. Ambrosiella, Raffaelea and Dryadomyces) and ultimately were derived from plant pathogens. The term ‘ambrosia’ refers to the mycelium of these fungi that both beetle adults and larvae feed on. This association is very intimate, with the beetles depending on the fungi for essential vitamins, amino acids and sterols. In contrast, bark beetles do not feed on fungi but on the sugar-rich phloem of trees. However, they need fungal symbionts to evade the tree’s resin or latex defences – the fungi grow so quickly that they block the canals through which these substances are secreted.

A particular ambrosia beetle species is usually associated with one strictly asexual primary fungus. Although this primary cultivar dominates, beetle gardens are typically not pure monocultures but assemblages of bacteria, yeasts and less specific auxiliary fungi (which are often sexual). Such secondary symbionts might help with obtaining nutrients from wood, but their exact role still remains unknown. The beetle gardeners are able to control growth and composition of the fungal crop. Weedy fungi might compete with the cultivar for nutrients or even turn into pathogens and are thus regularly removed by the beetles. As their gardens are relatively small, this can easily be done by a single female. In just the same way as in the attine ants, the risk of infection by pathogens is controlled not only by oral secretions but also by a symbiotic bacterium (an actinomycete). However, as gardening takes place in a closed system (the beetles forage inside the nest) and the tree heartwood or sapwood is virtually sterile, contamination is presumably a smaller problem than in ant or termite colonies.

Some beetles form a symbiosis with different primary fungi in different geographic regions, and sympatric beetles might share cultivars. Cultivar exchange could potentially occur, if fungi from one colony contaminate adjacent colonies of other females in the same tree. As in attine ants, the fungal cultivars of ambrosia beetles are transmitted vertically from one generation to the next. When female reproductives disperse, they carry inocula from their natal fungus garden and use them to start a new garden elsewhere (this sort of behaviour is known as trophophoresy). The fungal spores are transported in specialised pockets, the so-called mycangia. These deep and complex cuticular pouches are often lined with glands that secrete substances to support the spores, and setae at the entrance probably help with collecting spores. Mycangia are strikingly diverse, often occurring in different regions of the body in different species, and also rampantly convergent.

Evolutionary origins of farming

Molecular analyses showed that fungus gardening in ambrosia beetles has evolved at least seven times in different tribes between 20-60 million years ago – once in the ancestor of the Xyleborini about 30-40 million years ago and six times in several non-xyleborine lineages. It seems that in some cases, the beetles first served as a vector of a fungus, then began to derive nutrition from it, and finally cultivated it (transmission-first model), whereas in others, consumption of the fungus might have been the first step (consumption-first model). All origins of ambrosia feeding followed shifts from conifers to angiosperms, and there are no known cases in which agricultural lineages reversed to non-agricultural life. This suggests that the transition to fungiculture might constrain subsequent evolution.

Adaptations to farming

Ambrosia beetles show various specialisations for fungus farming, including mycangia, modifications of the larvae’s mandibles and guts for fungus-feeding and physiological as well as behavioural adaptations of adults for gardening. Specialisations in the fungi are harder to identify. The symbiotic fungi of ants and termites produce special nutrient-rich structures that can easily be harvested and consumed by their farmers, but no such structures have been found in the fungi associated with ambrosia beetles. However, the ambrosial growth, which consists of tightly packed conidiophores with abundant spores, occurs only in fungi that are farmed by beetles, suggesting evolutionary modifications for efficient consumption and digestion. Multiple lineages in the polyphyletic fungus genera Ambrosiella and Raffaelea have converged on a very similar ambrosial morphology.

Further convergences

All three insect groups with agriculture show some degree of sociality. While ants and termites are all eusocial, only one species of ambrosia beetle (Austroplatypus incompertus) has evolved eusociality. The others are subsocial or communal, and larval development depends on intense care by the adults. Sociality is likely to have facilitated the evolution of agriculture, as there is an inherent advantage of a division of labour. However, task partitioning remains largely unstudied in ambrosia beetles.

Also haplodiploidy, a sex determination system typical of most hymenopterans, has evolved in ambrosia beetles, and there are at least eight independent origins of extreme levels of inbreeding in the Scolytinae, probably facilitated by the close proximity of siblings during larval development.

Agriculture in other beetles

Whilst the ambrosia beetles tend to steal the show when it comes to coleopteran agriculture, such cultivation has evolved independently at least two more times.

Euops weevils

Females of the genus Euops in the weevil family Attelabidae show parental care in that they cut and roll a leaf to construct a cradle in which they lay a few eggs. The larvae then develop and pupate inside this cradle. The female nibbles the leaf in a regular pattern, thus creating small hollows in which she “sows” fungal spores (e.g. of Penicillium). The spores are distributed with the help of abdominal structures called comb plates and contained in three chambers on the female’s abdomen, referred to as ‘spore reservoir’, ‘spore incubator’ and ‘spore bed’. These chambers resemble the mycangia of ambrosia beetles (but they have only one type of mycangium). It seems that the spores are kept in good condition within the chambers, and as the chamber walls are lined with secretory cells, it has been suggested that spore development is controlled by substances produced by these cells. The symbiotic mycangial fungi then grow on the leaf and, initially, it was assumed that they enhance the leaf’s nutritional value by decomposing indigestible lignin and polysaccharides and increasing the soluble sugar content. However, this does not seem to be the case. Alternatively, the fungi, which produce antimicrobial compounds, could protect the larvae from harmful fungi or bacteria, but this remains to be shown.

Lymexylidae

Probably the first beetles to evolve agriculture were the Lymexylidae, a wood-boring group that contains the once-feared ship timber beetle. Lymexylid beetles have various associations with fungi, typically as a source of food, but one species has taken to farming these fungi. Female Hylecoetus dermestoides lay their eggs in cracks in the bark of dead or diseased trees. Each egg is coated with fungal spores that are stored in a mycangium-like pouch adjacent to the female’s ovipositor. Once hatched, the larvae pick up some of the spores and tunnel into the wood. Here, the fungus grows in a sheltered environment, and the larvae flourish on the ambrosial farms.