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

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.

Penetrative and non-penetrative interaction between Laboulbeniales fungi and their arthropod hosts

“…The micro-CT results from Arthrorhynchus agree perfectly with the previously known light microscope and transmission electron microscope images 2 . This emphasizes that microtomography is a good technique to visualize the type of fungal attachment to the host and especially the penetration of the cuticle, apart from the study of thallus in amber fossils 17 . As Jensen et al (2019) demonstrated the presence of a haustorium in Arthrorhynchus using scanning electron microscopy, we are confident that the lack of penetration and haustorium in Rickia found by micro-CT is real.…”

“…Laboulbeniales hosts must combine important properties: (i) successive generations of adult hosts should overlap in time because transmission occurs mainly during copulation, because the vast majority does not live on eggs or larval stages of their host; (ii) their populations must be large and stable; and (iii) they must inhabit moist environments 8 . Studies on Laboulbeniales have mostly been taxonomic, with a very recent emergence of phylogenetic analysis 9 – 13 , and a few recent studies have provided insights into the interaction of Laboulbeniales and their hosts, and the environment 2 , 14 – 17 .…”

Fossils of parasitic fungi

“…2F, G). Another fossil attributed to the Laboulbeniales with confidence has recently been discovered in Miocene Dominican amber (˜18 Ma) (Perreau et al ., 2021). This fungus, Columnomyces electri, occurs on the leg of a leiodid beetle, and its discovery indicated that these beetles and their parasitic Laboulbeniales have coevolved at least since the Miocene (Fig.…”

“…A fossil member of the order Laboulbeniales, which are obligate ectoparasites (Haelewaters et al ., 2021), is preserved on the thorax of a stalk-eyed fly in Bitterfeld amber (˜24 Ma) from Germany (Rossi et al ., 2005). The authors stated that the fungus is preserved in Baltic amber, but it is actually Bitterfeld amber (Perreau et al ., 2021). This fossil was assigned to the extant genus Stigmatomyces, of which representatives are parasites of Diptera, and described as S. succinii.…”

A second fossil species of the enigmatic rove beetle genusCharhyphusin Eocene Baltic amber, with implications on the morphology of the female genitalia (Coleoptera: Staphylinidae: Phloeocharinae)

“…Recently, non-destructive techniques have been used more frequently to examine amber inclusions based on 3D reconstructions (Penney 2016). The recent advancement of μ-CT and propagation phase-contrast X-ray synchrotron imaging has opened new windows for achieving high-quality reconstructions and individual X-ray sliced images for amber beetles (e.g., Chatzimanolis et al 2013;Zanetti et al 2016;Jałoszyn ´ski et al 2018Jałoszyn ´ski et al , 2020Bukejs et al 2020a, b;Shavrin & Kairišs 2020, 2021Alekseev et al 2021;Perreau et al 2021;Schmidt et al 2021). They are useful in excluding extra bubble layers surrounding the surfaces of inclusions (e.g., Yamamoto & Maruyama 2018;Kundrata et al 2020;Kypke & Solodovnikov 2020;Shavrin & Yamamoto 2020) and in removing certain extra body parts from reconstructions (e.g., Perreau & Tafforeau 2011;Bukejs et al 2020a, b).…”