Molecular phylogeny of bark and ambrosia beetles reveals multiple origins of fungus farming during periods of global warming

Abstract

Background: Fungus farming is an unusual life style in insects that has evolved many times in the wood boring weevils named 'ambrosia beetles'. Multiple occurrences of this behaviour allow for a detailed comparison of the different origins of fungus farming through time, its directionality, and possible ancestral states. We tested these hypotheses with a phylogeny representing the largest data set to date, nearly 4 kb of nucleotides from COI, EF-1α, CAD, ArgK, 28S, and 200 scolytine taxa.

Results: Phylogenetic analyses using Bayesian or parsimony approaches placed the root of Scolytinae close to the tribe Scolytini and Microborus, but otherwise indicated low resolution at older nodes. More recent clades were well resolved, including ten origins of fungus farming. There were no subsequent reversals to bark or phloem feeding in the fungus farming clades. The oldest origin of fungus farming was estimated near 50 Ma, long after the origin of Scolytinae (100-120 Ma). Younger origins included the species rich Xyleborini, dated to 21 Ma. Sister group comparisons and test of independence between traits indicated that neither gregarious larval feeding nor regular inbreeding by sibling mating was strongly correlated with the origin of fungus farming.

Conclusion: Origins of fungus farming corresponded mainly with two periods of global warming in the Cenozoic era, which were characterised by broadly distributed tropical forests. Hence, it seems likely that warm climates and expanding tropical angiosperm forests played critical roles in the successful radiation of diverse fungus farming groups. However, further investigation will likely reveal additional biological factors that promote fungus farming.

Figure 1

Molecular phylogeny of Scolytinae. Topology based on Bayesian analysis of 3,694 nucleotides from five unlinked gene fragments, using seven unlinked data partitions (mtDNA positions 1, 2, and 3, nucDNA protein encoding gene positions 1, 2, and 3, 28S rRNA). Posterior probability marked on nodes by ** = 100, * = > 95. Obligate fungus farming is marked in blue, with blue hatch mark signifying ambrosia symbiosis in a single species. Red dots indicate the inferred origin of regular sibling mating.

Figure 2

Dates of origins of key evolutionary traits in Scolytinae. Age of gregarious larval feeding (G), regular inbreeding by sibling mating (thin line), and ambrosia fungus feeding (grey box) in Scolytinae, based on crown ages as estimated in Beast (Analysis A). Stippled line and light grey indicate uncertainties associated with the lack of observations (Bothrosternini) or lack of phylogenetic sampling (Hyorrhynchini). Only those larvae that move freely and feed gregariously are considered truly ‘gregarious.’ Above, the Zachos curve showing variation in global temperature, and the posterior 95% distribution of crown age for Corthylina, Xyloterini, Scolytoplatypus, Camptocerus, Xyleborini, and the Bothrosternus-Eupagiocerus clade.