Rediscovery of the enigmatic fungus-farming ant "Mycetosoritis" asper Mayr (Hymenoptera: Formicidae): Implications for taxonomy, phylogeny, and the evolution of agriculture in ants

Abstract

We report the rediscovery of the exceedingly rarely collected and enigmatic fungus-farming ant species Mycetosoritis asper. Since the description of the type specimen in 1887, only four additional specimens are known to have been added to the world's insect collections. Its biology is entirely unknown and its phylogenetic position within the fungus-farming ants has remained puzzling due to its aberrant morphology. In 2014 we excavated and collected twenty-one colonies of M. asper in the Floresta Nacional de Chapecó in Santa Catarina, Brazil. We describe here for the first time the male and larva of the species and complement the previous descriptions of both the queen and the worker. We describe, also for the first time, M. asper biology, nest architecture, and colony demographics, and identify its fungal cultivar. Molecular phylogenetic analyses indicate that both M. asper and M. clorindae are members of the genus Cyphomyrmex, which we show to be paraphyletic as currently defined. More precisely, M. asper is a member of the Cyphomyrmex strigatus group, which we also show to be paraphyletic with respect to the genus Mycetophylax. Based on these results, and in the interest of taxonomic stability, we transfer the species M. asper, M. clorindae, and all members of the C. strigatus group to the genus Mycetophylax, the oldest available name for this clade. Based on ITS sequence data, Mycetophylax asper practices lower agriculture, cultivating a fungal species that belongs to lower-attine fungal Clade 2, subclade F.

Fig 1. Phylogeny of fungus-farming ants based on Bayesian analysis of five nuclear protein-coding genes.

Mycetophylax asper is indicated in red. Red box indicates our newly expanded definition of the genus Mycetophylax (see text for details).

Fig 2. The queen (holotype) and first-described worker of Mycetophylax asper.

a) Queen, full-face view; b) worker, full-face view; c) queen, lateral profile; d) worker, lateral profile; e) queen, dorsal view; f) worker, dorsal view; g) queen, specimen labels; h) worker, specimen labels.

Fig 3. Worker, queen, and male of Mycetophylax asper.

a) Worker, lateral profile; b) worker, dorsal view; c) queen, lateral profile; d) queen, dorsal view; e) male, lateral profile; f) male, dorsal view; g) worker, full-face view; h) queen, full-face view; i) male, full-face view.

Fig 4. Worker, queen, and male of Mycetophylax asper, SEM images.

a) Worker, full-face view; b) queen, full-face view; c) male, full-face view; d) worker head, lateral view; e) queen head, lateral view; f) male head, lateral view; g) worker mesosoma, lateral profile; h) queen mesosoma, lateral profile; i) male mesosoma, lateral profile; j) worker, dorsal view; h) queen, dorsal view; i) male, dorsal view.

Fig 5. Morphological details of Mycetophylax asper, SEM images.

a) Worker, mandibles; b) queen, mandibles; c) worker, propleural plates; d) worker, dorsal view of petiole, postpetiole, and gastral tergite I; e) worker, hind leg showing the ventral femoral carina.

Fig 6. Wings of Mycetophylax asper.

a) Queen, fore and hind wings; b) male, fore and hind wings. Scale bars in figures represent 1.0 mm in length.

Fig 7. Prepupal worker larva of Mycetophylax asper, SEM images.

a) Lateral profile; b) and c) head, full-face view; d) mouthparts; e) thorax, ventral view; f) ventral view; g) anal opening (venter at top).

Fig 8. Mycetophylax asper, field images.

a) Nest entrance, nest TRS141017-01; b) nest entrance, nest AJ141018-11; c) subterranean garden chamber; d) fungus garden and ants in field nest boxes; e) fungus garden and ants in field boxes showing pellet of wet dirt or refuse; g) and f) habitat.

Fig 9. Fungal phylogeny based on Bayesian analysis of ITS sequences.

Terminal taxa are named by their ant host species or genera except for free-living Lepiotaceae. Letters F, E, and G refer to subclades of fungal cultivar Clade 2, as defined in Mehdiabadi et al., [41]. Photographs courtesy of: Karolyn Darrow (top) and Don Parsons (bugpix@charter.net) (bottom).