Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences

Abstract

Among fungi, the basic life strategies are saprophytism, parasitism, and predation. Fungi in Orbiliaceae (Ascomycota) prey on animals by means of specialized trapping structures. Five types of trapping devices are recognized, but their evolutionary origins and divergence are not well understood. Based on comprehensive phylogenetic analysis of nucleotide sequences of three protein-coding genes (RNA polymerase II subunit gene, rpb2; elongation factor 1-alpha gene, ef1-alpha; and ss tubulin gene, bt) and ribosomal DNA in the internal transcribed spacer region, we have demonstrated that the initial trapping structure evolved along two lineages yielding two distinct trapping mechanisms: one developed into constricting rings and the other developed into adhesive traps. Among adhesive trapping devices, the adhesive network separated from the others early and evolved at a steady and gentle speed. The adhesive knob evolved through stalk elongation, with a final development of nonconstricting rings. Our data suggest that the derived adhesive traps are at a highly differentiated stage. The development of trapping devices is felicitous proof of adaptive evolution.

Fig. 1.

Trapping devices of the Orbiliaceae. (A) AN. (B) AK with NCR. (C) AC. (D) CR. (Scale bar, 10 μm.)

Fig. 2.

Parsimony analyses of ITS regions (A) and combined data sets (B). Bootstrap values were obtained from 1,000 replications, and only >50% are shown.

Fig. 3.

ML tree of combined sequences with GTR+Γ+I model and character evolution reconstructed using parsimony. The characters of trapping devices are associated with each taxon. The numbers above each branch show the ME BSV after 1,000 replications. Dr., Drechslerella; A., Arthrobotrys; D., Dactylellina; V., Vermispora; SSK, simple sessile knobs; SK, stalked knobs; SK and proliferating knob (PK), stalked knobs with PK; SK and NCR, stalked knobs with NCR; OUT, outgroups without traps.

Fig. 4.

Comparison of three hypotheses on the evolution of fungal nematode-trapping devices in the Orbiliaceae. SS, specialized structure; SiK, simple knob; SK, stalked knob; PK, chain of proliferating knob; *, adhesive column with globose terminal cell. Lower Left, see ref. ; Lower Right, see ref. .