A parasitic coevolution since the Miocene revealed by phase-contrast synchrotron X-ray microtomography and the study of natural history collections

Paul Tafforeau,Michel Perreau,Danny Haelewaters

doi:10.1038/s41598-020-79481-x

Abstract

The discovery of a new fossil species of the Caribbeo-Mexican genus Proptomaphaginus (Coleoptera, Leiodidae, Cholevinae) from Dominican amber, associated with a new fossil parasitic fungus in the genus Columnomyces (Ascomycota, Laboulbeniales), triggered an investigation of extant species of Proptomaphaginus and revealed the long-enduring parasitic association between these two genera. This effort resulted in the description of the fossil species †Proptomaphaginus alleni sp. nov., and one fossil and two extant species of Columnomyces, selectively associated with species of Proptomaphaginus: †Columnomyces electri sp. nov. associated with the fossil †Proptomaphaginus alleni in Dominican amber, Columnomyces hispaniolensis sp. nov. with the extant Proptomaphaginus hispaniolensis (endemic of Hispaniola), and Columnomyces peckii sp. nov. with the extant Proptomaphaginus puertoricensis (endemic of Puerto Rico). Based on biogeography, our current understanding is that the Caribbean species of Proptomaphaginus and their parasitic species of Columnomyces have coevolved since the Miocene. This is the first occurrence of such a coevolution between a genus of parasitic fungus and a genus of Coleoptera. The phylogenetic relations among Proptomaphaginus species are also addressed based on a parsimony analysis. Fossil specimens were observed by propagation phase-contrast synchrotron X-ray microtomography (PPC-SRμCT) and extant specimens were obtained through the study of preserved dried, pinned insects, attesting for the importance of (i) technological advancement and (ii) natural history collections in the study of microparasitic relationships.

Highlights

There is scientific consensus for the idea that the number of fungal parasites is highly underestimated[1,2,3,4,5,6]
The first morphology-based phylogeny of the extant species of Proptomaphaginus was presented by P eck[26]. We extended his analysis to include the newly described fossil species and the two most species-rich Asian genera that belong to the same subtribe of Ptomaphagini, Ptomaphaginina
Four species are recognized in the genus Columnomyces—one fossil species and three extant species

Summary

Introduction

There is scientific consensus for the idea that the number of fungal parasites is highly underestimated[1,2,3,4,5,6]. 1.5% of insect-associated fungi are thought to be currently known[5] These include necrotrophic and biotrophic parasites[7]. Certain phytopathogens can be hemibiotrophic parasites—they require a living host, which is killed at later stages of infection An example of this type of parasitism is Magnaporthe grisea (Sordariomycetes, Magnaporthales). One fossil species has been reported in the literature This is †Stigmatomyces succini, a parasite of the fly †Prosphyracephala succini (Diptera, Diopsidae)[14]. Extant species of Ptomaphagini (Coleoptera, Leiodidae, Cholevinae) are reported to host representatives of three genera of Laboulbeniales: Columnomyces on a Nearctic species of Ptomaphagus[19]; Diphymyces on species of Adelopsis[21,22], Ptomaphagus[22,23], and Ptomaphaginus[24]; and Rodaucea on species of Adelopsis[22,25]. An undescribed species has been reported from the Bahamas[27], extending the northern latitudinal limit of the distribution area of the genus to 25° N

Methods

Results

Discussion

Conclusion