Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations

Abstract

The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position-induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.

Keywords: Ascomycota; ectoparasites; host specialization; phenotypic plasticity; ribosomal DNA; taxonomy.

Figure 1

(a) Arthrorhynchus nycteribiae. (b) Gloeandromyces streblae. (c) Nycteromyces streblidinus, a female thallus

Figure 2

Field sites where bat flies for this project have been collected. Field sites are located in North and Central America (Costa Rica, Honduras, Mexico, Nicaragua, Panama), South America (Ecuador, Trinidad), and Europe (Croatia, Hungary, Slovakia, Portugal, Spain)

Figure 3

Maximum clade credibility tree, reconstructed from the concatenated SSU + LSU dataset. The tree is the result of a Bayesian analysis performed in BEAST. For each node, ML BS (if ≥70)/Bayesian pp (if ≥0.7) are presented above to the branch leading to that node. The arrowheads denote the Stigmatomycetinae subtribe sensu Tavares (1985)

Figure 4

Maximum clade credibility tree showing species in the genus Gloeandromyces, with Stigmatomyces protrudens as outgroup. The tree is the result of a Bayesian analysis of the LSU dataset performed in BEAST. For each node, ML BS (if ≥70)/Bayesian pp (if ≥0.7) are presented above the branch leading to that node. At the right, thalli are shown of the different morphologies observed. From top to bottom: Gloeandromyces nycteribiidarum, G. sp. nov. 3, G. streblae (left) and G. sp. nov. 2 (right), G. pageanus, G. sp. nov. 1 (left), and G. sp. nov. 4 (right)

Figure 5

Host–parasite–parasite network of the final temperate dataset. Shown is the association of bat flies with their bat hosts (left) as well as the association of Laboulbeniales (right) and their bat fly hosts. Bar width represents the relative abundance of a species within each network level

Figure 6

Host–parasite–parasite network of the final neotropical dataset. Shown is the association of bat flies with their bat hosts (left) as well as the association of Laboulbeniales (right) and their bat fly hosts. Bar width represents the relative abundance of a species within each network level

Figure 7

Co‐phylogenetic relationships between bat flies and Laboulbeniales. Maximum likelihood phylogenies for bat flies (left) and their Laboulbeniales parasites (right). For each node, ML BS (if ≥70) are presented above the branch leading to that node. All associations are shown as gray connecting lines. Old World bat flies and Laboulbeniales are highlighted in green. Penicillidia monoceros substituted for Penicillidia dufourii

Figure 8

Comparison of two species of Laboulbeniales. Left. Mature thallus of Cupulomyces lasiochili, reproduced from Benjamin (1992a). Right. Mature thallus of Prolixandromyces rhinoceralis, reproduced from Benjamin (1981). Annotated are cells I, II, III, and VI, and tiers of perithecial outer wall cells (w¹ to w⁵)