Unexpected cryptic species diversity of parasites of the family Xenidae (Strepsiptera) with a constant diversification rate over time

Abstract

Parasitism is one of the most successful and ancient strategies. Due to the specialized lifestyle of parasites, they are usually affected by reductions and changes in their body plan in comparison with nonparasitic sister groups. Extreme environmental conditions may impose restraints on behavioural or physiological adaptations to a specific host and limit morphological changes associated with speciation. Such morphological homogeneity has led to the diversity of parasites being underestimated in morphological studies. By contrast, the species concept has dramatically changed in many parasitic groups during recent decades of study using DNA sequence data. Here we tested the phenomenon of cryptic species diversity in the twisted‐wing parasite family Xenidae (Strepsiptera) using nuclear and mitochondrial DNA sequence data for a broad sample of Xenidae. We used three quantitative methods of species delimitation from the molecular phylogenetic data – one distance‐based (ABGD) and two tree‐based (GMYC, bPTP). We found 77–96 putative species in our data and suggested the number of Xenidae species to be more diverse than expected. We identified 67 hosts to species level and almost half of them were not previously known as hosts of Xenidae. The mean number of host species per putative species varied between 1.39 and 1.55. The constant rate in net diversification can be explained by the flexibility of this parasitic group, represented by their ability to colonize new host lineages combined with passive long‐range dispersal by hosts.

Xenos yangi sp. nov.: A new twisted-wing parasite species (Strepsiptera, Xenidae) from Gaoligong Mountains, Southwest China

“…For the other lineages including specimens identified as X. minor, X. vesparum and X. ropalidiae, we noticed that X. minor and X. vesparum form a clade including four groups (group 6, 7, 8 and 9) (Fig. 6) and their genetic divergences are less than 0.007 (Table 2), suggesting these specimens may be the same species (Benda et al 2021). On the other hand, different populations (Laos, Nepal, Malaysia) of X. ropalidiae form two separate groups (5 and 10) with a genetic divergence of 0.368-0.421 (Table 2), which may include different species (Benda et al 2021).…”

“…Combined with 45 COI sequences of Xenos published by others (Carapelli et al 2006;McMahon et al 2011;Nakase and Kato 2013;Jůzová et al 2015;Benda et al 2021), phylogenetic analyses were performed using maximum likelihood (ML), and maximum parsimony (MP) methods with four strepsipteran species Stylops ater Reichert, 1914, Melittostylops hesperapium Kinzelbach, 1971, Halictoxenos tumulorum Perkins, 1918 and Crawfordia warnckei Kinzelbach, 1970 (Stylopidae) (GenBank Accession: GAZM00000000.2, MK431155, KF803415, MK431154) as outgroups (Misof et al 2014;Jůzová et al 2015;Benda et al 2019 ). Briefly, COI sequences were first translated to amino acid sequences with the invertebrate mitochondrial genetic code, and then aligned by codons using the ClustalW algorithm in MEGA-X v10.1.8 (Sudhir et al 2018).…”

“…Information on the other seven Xenos species (X. oxyodontes, X. moutoni, X. vespularum, X. pecki, X. vesparum, X. ropalidiae, X. minor) in the phylogenetic analysis was obtained from previous reports (Carapelli et al 2006;McMahon et al 2011;Nakase and Kato 2013;Jůzová et al 2015;Benda et al 2019Benda et al , 2021. In detail, male and neotenic females of X. oxyodontes (COI GenBank accessions number: AB759562-AB759569; JN082805; MK431184; MN914546) were collected from Japan and Korea (McMahon et al 2011;Nakase and Kato 2013;Benda et al 2019Benda et al , 2021; male pupa, males and neotenic females of X. moutoni (COI GenBank accessions number: AB759570-AB759582, MN914545, MK431183) were collected from China, Japan and Laos (Nakase and Kato 2013;Benda et al 2019Benda et al , 2021; two males of X. vespularum (COI GenBank accessions number: AB759583; MK431222) were collected from Japan (Nakase and Kato 2013;Benda et al 2021); male and neotenic females of X. pecki (COI GenBank accessions number: MN914547-MN914549; MK431187) were collected from USA (Benda et al 2019(Benda et al , 2021; male and neotenic females of X. vesparum (COI GenBank accessions number: DQ364229.1; KF803535.1; MN914557; JN082806; MN914561; MK431205) were collected from Italy, Czech Republic, Austria (Carapelli et al 2006;Jůzová et al 2015;Benda et al 2019Benda et al , 2021; two neotenic females of X. ropalidiae (COI GenBank accessions number: MK431185-MK431186) were collected from Laos and Nepal, and two males of X. ropalidiae (COI GenBank accessions number: MK431189-MK431190) were collected from Malaysia (Benda et al 2019); and male and neotenic females of X. minor (COI GenBank accessions number: MN914559-MN914560; MN914569) were collected from Croatia (Benda et al 2021).…”

The genus Bilharziella vs. other bird schistosomes in snail hosts from one of the major recreational lakes in Poland

“…Morphological similarity to the later on one hand and considerable genetic divergence between them strongly suggest the presence of a cryptic species which is not surprising phenomenon especially in case of parasites (e.g. Hanelt et al, 2015;Cai et al, 2020;Benda et al, 2021).…”

More than meets the eye: decrypting diversity reveals hidden interaction specificity between frogs and frog‐biting midges

“…Despite a vast and increasing number of studies, the species richness of many insect communities remains highly uncertain, partly due to a large degree of cryptic, i.e morphologically indistinguishable but genetically distinct, species (Bickford et al ., 2007), especially among many parasitic taxa (e.g. Poulin, 2011a; Pérez‐Ponce de León & Nadler, 2016; Benda et al ., 2021), with potential implications for epidemiology, diagnostics, and our understanding of trophic network topology.…”