Sociality in fungus cultivating beetles

Eusocial organisms, where many individuals in a population abstain from reproduction lifelong, represent the pinnacle of social evolution. This ultimate form of “reproductive altruism” is found in several insects including ants, termites, wasps and bees as prime examples. Its evolution can be studied in taxa that share the ecological conditions with eusocial species without having attained this ultimate level of sociality.

Ambrosia beetles are a speciose group of bark beetles in the subfamily Scolytinae that share with fungus-growing ants and termites their full dependence on fungus agriculture. Furthermore, the xyleborine ambrosia beetles are haplodiploid like eusocial hymenoptera, show extraordinary inbreeding levels enhancing relatedness among colony members, and live inside their larder (tree trunks) like eusocial termites. Despite combining such crucial features of the biology and ecology of eusocial insects, ambrosia beetles are not eusocial, which renders them an ideal model for the study of the evolutionary mechanisms leading to eusociality.

The term ‘ambrosia’ refers to the fungi cultivated by the beetles on their gallery walls, upon which they feed. This mutualism provides beetles with a rich and steady harvest of fungal fruiting bodies, and the fungi in turn with an efficient distribution system, as dispersing beetles carry fungal spores in specific organs (mycangia) used as a head start in their newly founded galleries.

Our research on three species of European ambrosia beetles hitherto revealed that full-sib mating is virtually the rule (97% in Xylosandrus germanus) yielding exceptional inbreeding levels, which is associated with a striking outbreeding depression. Nevertheless, females still adjust the sex ratio of their offspring to the rare outbreeding opportunities of their sons. Daughters stay in their maternal gallery to help raising sisters, which reduces their own reproductive potential. Most colony members disperse to start breeding independently at some stage, classifying this system as “cooperative breeding” and not eusocial, i.e. there is no lifelong reproductive sacrifice. Why this is the case is a puzzle we are trying to solve.

Within the maternal colony, offspring fulfil divergent tasks with a clear division of labour, particularly between larvae that enlarge the gallery by chewing up wood, and adults that tend the fungi, while both larvae and adults show specific maintenance behaviours serving gallery hygiene and immune defence. Dispersal decisions of adult females depend on intrinsic colony parameters like the need for help and the reproductive status of the breeding female, and on extrinsic factors influencing dispersal conditions like local weather prospects. Artificial selection for delayed dispersal renders increased alloparental investment, revealing genetic linkage between the fundamental components of cooperative breeding: delayed dispersal and alloparental care.

Principal investigator: Michael Taborsky

Sample publications:

Nuotclà, J.A., Diehl, J.M.C, Taborsky, M. 2021. Habitat Quality Determines Dispersal Decisions and Fitness in a Beetle – Fungus Mutualism. Front. Ecol. Evol. 9:602672 [PDF]

Nuotclà, J. A., Biedermann P. H. W., Taborsky, M. (2019) Pathogen defence is a potential driver of social evolution in ambrosia beetles. Proc. R. Soc. B 286: 20192332 [PDF]

Biedermann P.H.W. & Taborsky M. (2011): Larval helpers and age polyethism in ambrosia beetles. Proc Natl Acad Sci USA108:17064-17069 [PDF]

Biedermann P.H.W., Klepzig K.D. & Taborsky M. (2011): Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae). Behavioral Ecology & Sociobiology 65:1753–1761 [PDF]

Peer K. & Taborsky M. (2005) Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sib mating. Evolution 59, 317-323 [PDF]