Origin and evolution of carnivorism in the Ascomycota (fungi)

Abstract

Carnivorism is one of the basic life strategies of fungi. Carnivorous fungi possess the ability to trap and digest their preys by sophisticated trapping devices. However, the origin and development of fungal carnivorism remains a gap in evolution biology. In this study, five protein-encoding genes were used to construct the phylogeny of the carnivorous fungi in the phylum Ascomycota; these fungi prey on nematodes by means of specialized trapping structures such as constricting rings and adhesive traps. Our analysis revealed a definitive pattern of evolutionary development for these trapping structures. Molecular clock calibration based on two fossil records revealed that fungal carnivorism diverged from saprophytism about 419 Mya, which was after the origin of nematodes about 550-600 Mya. Active carnivorism (fungi with constricting rings) and passive carnivorism (fungi with adhesive traps) diverged from each other around 246 Mya, shortly after the occurrence of the Permian-Triassic extinction event about 251.4 Mya. The major adhesive traps evolved around 198-208 Mya, which was within the time frame of the Triassic-Jurassic extinction event about 201.4 Mya. However, no major carnivorous ascomycetes divergence was correlated to the Cretaceous-Tertiary extinction event, which occurred more recently (about 65.5 Mya). Therefore, a causal relationship between mass extinction events and fungal carnivorism evolution is not validated in this study. More evidence including additional fossil records is needed to establish if fungal carnivorism evolution was a response to mass extinction events.

Fig. 1.

Bayesian-inferred phylogenetic tree of carnivorous Orbiliomycetes by five protein-coding genes. The tree was constructed by MrBayes with a portioned strategy. All associated parameters were unlinked. The topology was also tested by a 1,000 bootstrap maximum-likelihood analysis; the bootstrap value is marked on the branch. The branches with a bootstrap value lower than 70% are not shown. Trapping devices are drawn on the left. SSK, sessile adhesive knob; SK, stalked adhesive knob; AN, adhesive net; AC, adhesive column; NCR, nonconstricting ring; CR, constricting ring.

Fig. 2.

Estimated divergence times of the major lineages in the carnivorous Orbiliomycetes. Chronogram was constructed using BEAST based on the Bayesian-inferred tree with three calibrations: root node (300–500 Mya), node A (100–500 Mya), and node B (24–500 Mya). Deep-branching phylogeny illustrating the relationships among different lineages is shown by different colors. Error bars are shown and each represents the 95% highest posterior density (HPD) for a node age. The red lines “a” and “b” represent the mass extinction events of the Permian–Triassic (251.4 Mya) and the Triassic–Jurassic (201.4 Mya), respectively. The orange line “c” represents the mass extinction event of the Cretaceous–Tertiary (65.5 Mya). Nodes A and B indicate the two fossil calibration nodes. SSK, sessile adhesive knob; SK, stalked adhesive knob; AN, adhesive net; AC, adhesive column; NCR, nonconstricting ring; CR, constricting ring.

Fig. 3.

The origin time of Pezizomycotina with 1,069 orthologs. Three calibrations were applied to the two alternative topologies. The root node was calibrated between 452 and 1,489 Mya. The last common ancestor (LCA) of Nectriaceae, Clavicipitaceae, and Hypocreaceae was calibrated between 150 and 213 Mya. The divergence of Clavicipitaceae and Hypocreaceae was calibrated between 146 and 206 Mya. Error bars are shown, each representing the 95% highest posterior density (95% HPD) for a node age. Geological times are provided on the median axis. SSK, sessile adhesive knob; SK, stalked adhesive knob; AN, adhesive net; AC, adhesive column; NCR, nonconstricting ring; CR, constricting ring. (A) Orbiliomycetes is used as the basal group of Pezizomycotima with Pezizomycetes diverging afterward. (B) Pezizomycetes is used as the basal group with Orbiliomycetes diverging afterward.