Are fleas highly modified Mecoptera? Phylogenomic resolution of Antliophora (Insecta: Holometabola)

Abstract

Insect orders have been defined and stable for decades, with few notable exceptions (e.g., Blattodea and Psocoptera). One of the few remaining questions of order-level monophyly is that of Mecoptera in respect to the phylogenetic placement of Siphonaptera (fleas). We used a large set of transcriptomic nucleotide sequence data representing 56 species and more than 3,000 single-copy genes to resolve the evolutionary history of Antliophora, including fleas (Siphonaptera), scorpionflies and relatives (Mecoptera), and true flies (Diptera). We find that fleas and mecopterans together are the sister group of flies. However, our data and/or analyses are unable to distinguish whether fleas are sister to a monophyletic Mecoptera, or whether they arose from within extant mecopteran families, rendering Mecoptera paraphyletic. We did not detect parameter bias in our dataset after applying a broad range of detection methods. Counter to a previous hypothesis that placed fleas within Mecoptera as the sister group to wingless boreids (snow fleas), we found a potential sister group relationship between fleas and the enigmatic family Nannochoristidae. Although we lack conclusive evidence, it seems possible that fleas represent the most-species rich group of modern mecopterans and that their parasitic lifestyle and morphological adaptations have simply made them unrecognizable in respect to their order-level classification.

Phylogenomic Subsampling and the Search for Phylogenetically Reliable Loci

“…Phylogenetic inference using subsampled data sets was performed using IQ-TREE 1.6.3 ( Nguyen et al 2015 ) under the LG+F + G model, and node support was estimated using 1,000 replicates of ultrafast bootstrap (UFBoot; Hoang et al 2018 ). Characterizing the performance of these data sets is complicated by the fact that the underlying phylogenies are unknown (in fact some of the trees used here have already been challenged to some degree; see Meusemann et al 2020 ; Szucsich et al 2020 ; Tihelka et al 2020) . Although large phylogenomic data sets generally produce fully resolved and supported topologies, model violations can favor incorrect trees ( Delsuc et al 2005 ; KapLi et al 2021) .…”

Phylogenetic resolution of the fly superfamily Ephydroidea–Molecular systematics of the enigmatic and diverse relatives of Drosophilidae

“…In particular, many lineages of parasites have been especially difficult to place phylogenetically using morphological characters. Classic examples abound in the insects [1], flowering plants [2], bacteria [3], fungi [4,5] and other metazoans [6]. Although many of these "orphan" lineages have found a home in the era of molecular systematics [7][8][9], even large phylogenomic data sets are sometimes unable to resolve challenging phylogenetic questions surrounding these lineages [1].…”

“…Classic examples abound in the insects [1], flowering plants [2], bacteria [3], fungi [4,5] and other metazoans [6]. Although many of these "orphan" lineages have found a home in the era of molecular systematics [7][8][9], even large phylogenomic data sets are sometimes unable to resolve challenging phylogenetic questions surrounding these lineages [1]. That these puzzles persist has been variously attributed to rapid radiations, adaptations that obscure groundplan synapomorphies and unpredictable conflict among data types.…”

The new Checklist of the Italian Fauna: Mecoptera

“…The order is peculiar for this reason, with seven of its nine extant families having one to a score of species, with the remaining two families -Bittacidae, with essentially a Southern Hemisphere distribution (and possible Gondwanan origin), and Panorpidae, with mostly a Northern Hemisphere distribution (and possible Laurasian origin) -containing 91% of the species. Moreover, it is subject of debate whether the Mecoptera form a single clade, or whether the Siphonaptera (fleas) are inside that clade, so that the traditional "Mecoptera" is paraphyletic (Meusemann et al 2020). Concerning the present checklist, scorpionflies are here considered in their traditional meaning, without the inclusion of Siphonaptera, considering three families observed in Italy, i.e.…”