Phylogenomic analysis of Stylops reveals the evolutionary history of a Holarctic Strepsiptera radiation parasitizing wild bees.

Holarctic Stylops is the largest genus of the enigmatic insect order Strepsiptera, twisted winged parasites. Members of Stylops are obligate endoparasites of Andrena mining bees and exhibit extreme sexual dimorphism typical of Strepsiptera. So far, molecular studies on Stylops have focused on questions on species delimitation. Here, we utilize the power of whole genome sequencing to infer the phylogeny of this morphologically challenging genus from thousands of loci. We use a species tree method, concatenated maximum likelihood analysis and Bayesian analysis with a relaxed clock model to reconstruct the phylogeny of 46 Stylops species, estimate divergence times, evaluate topological consistency across methods and infer the root position. Furthermore, the biogeographical history and coevolutionary patterns with host species are assessed. All methods recovered a well resolved topology with close to all nodes maximally supported and only a handful of minor topological variations. Based on the result, we find that included species can be divided into 12 species groups, seven of them including only Palaearctic species, three Nearctic and two were geographically mixed. We find a strongly supported root position between a clade formed by the spreta, thwaitesi and gwynanae species groups and the remaining species and that the sister group of Stylops is Eurystylops or Eurystylops + Kinzelbachus. Our results indicate that Stylops originated in the Western Palaearctic or Western Palaearctic and Nearctic in the early Neogene or late Paleogene, with four independent dispersal events to the Nearctic. Cophylogenetic analyses indicate that the diversification of Stylops has been shaped by both significant coevolution with the mining bee hosts and host-shifting. The well resolved and strongly supported phylogeny will provide a valuable phylogenetic basis for further studies into the fascinating world of Strepsipterans.

A generic classification of Xenidae (Strepsiptera) based on the morphology of the female cephalothorax and male cephalotheca with a preliminary checklist of species.

The generic taxonomy and host specialization of Xenidae have been understood differently by previous authors. Although the recent generic classification has implied a specialization on the level of host families or subfamilies, the hypothesis that each xenid genus is specialized to a single host genus was also previously postulated. A critical evaluation of the classification of the genera of Xenidae is provided here based on morphology in accordance with results of recent molecular phylogenetic studies. External features of the female cephalothoraces and male cephalothecae were documented in detail with different techniques. Diagnoses and descriptions are presented for all 13 delimited genera. The earliest diverging genera are usually well characterized by unique features, whereas deeply nested genera are usually characterized by combinations of characters. Three new genera are described: Sphecixenos gen. nov., Tuberoxenos gen. nov., and Deltoxenos gen. nov. Five previously described genera are removed from synonymy: Tachytixenos Pierce, 1911, stat. res.; Brasixenos Kogan & Oliveira, 1966, stat. res.; Leionotoxenos Pierce, 1909, stat. res.; Eupathocera Pierce, 1908, stat. res.; and Macroxenos Schultze, 1925, stat. res. One former subgenus is elevated to generic rank: Nipponoxenos Kifune & Maeta, 1975, stat. res. Monobiaphila Pierce, 1909, syn. nov. and Montezumiaphila Brèthes, 1923, syn. nov. are recognized as junior synonyms of Leionotoxenos Pierce, 1909, stat. res. Ophthalmochlus Pierce, 1908, syn. nov., Homilops Pierce, 1908, syn. nov., Sceliphronechthrus Pierce, 1909, syn. nov., and Ophthalmochlus (Isodontiphila) Pierce, 1919, syn. nov. are recognized as junior synonyms of Eupathocera Pierce, 1908, stat. res. A preliminary checklist of 119 described species of Xenidae with information on their hosts and distribution is provided. The following 14 species are recognized as valid and restituted from synonymy: Tachytixenosindicus Pierce, 1911, stat. res.; Brasixenosacinctus Kogan & Oliveira, 1966, stat. res.; Brasixenosaraujoi (Oliveira & Kogan, 1962), stat. res.; Brasixenosbahiensis Kogan & Oliveira, 1966, stat. res.; Brasixenosbrasiliensis Kogan & Oliveira, 1966, stat. res.; Brasixenosfluminensis Kogan & Oliveria, 1966, stat. res.; Brasixenosmyrapetrus Trois, 1988, stat. res.; Brasixenoszikani Kogan & Oliveira, 1966, stat. res.; Leionotoxenoshookeri Pierce, 1909, stat. res.; Leionotoxenosjonesi Pierce, 1909, stat. res.; Leionotoxenoslouisianae Pierce, 1909, stat. res.; Eupathoceraluctuosae Pierce, 1911, stat. res.; Eupathoceralugubris Pierce, 1909, stat. res.; Macroxenospiercei Schultze, 1925, stat. res. New generic combinations are proposed for 51 species: Leionotoxenosarvensidis (Pierce, 1911), comb. nov.; Leionotoxenosbishoppi (Pierce, 1909), comb. nov.; Leionotoxenosforaminati (Pierce, 1911), comb. nov.; Leionotoxenosfundati (Pierce, 1911), comb. nov.; Leionotoxenoshuastecae (Székessy, 1965), comb. nov.; Leionotoxenositatiaiae (Trois, 1984), comb. nov.; Leionotoxenosneomexicanus (Pierce, 1919), comb. nov.; Leionotoxenosprolificum (Teson & Remes Lenicov, 1979), comb. nov.; Leionotoxenosrobertsoni (Pierce, 1911), comb. nov.; Leionotoxenostigridis (Pierce, 1911), comb. nov.; Leionotoxenosvigili (Brèthes, 1923), comb. nov.; Eupathoceraargentina (Brèthes, 1923), comb. nov.; Eupathoceraauripedis (Pierce, 1911), comb. nov.; Eupathocerabucki (Trois, 1984), comb. nov.; Eupathoceraduryi (Pierce, 1909), comb. nov.; Eupathoceraerynnidis (Pierce, 1911), comb. nov.; Eupathocerafasciati (Pierce, 1909), comb. nov.; Eupathocerafuliginosi (Brèthes, 1923), comb. nov.; Eupathocerainclusa (Oliveira & Kogan, 1963), comb. nov.; Eupathocerainsularis (Kifune, 1983), comb. nov.; Eupathoceramendozae (Brèthes, 1923), comb. nov.; Eupathocerapiercei (Brèthes, 1923), comb. nov.; Eupathocerastriati (Brèthes, 1923), comb. nov.; Eupathocerataschenbergi (Brèthes, 1923), comb. nov.; Eupathocerawestwoodii (Templeton, 1841), comb. nov.; Macroxenospapuanus (Székessy, 1956), comb. nov.; Sphecixenosabbotti (Pierce, 1909), comb. nov.; Sphecixenosastrolabensis (Székessy, 1956), comb. nov.; Sphecixenosdorae (Luna de Carvalho, 1956), comb. nov.; Sphecixenoserimae (Székessy, 1956), comb. nov.; Sphecixenosesakii (Hirashima & Kifune, 1962), comb. nov.; Sphecixenosgigas (Pasteels, 1950), comb. nov.; Sphecixenoskurosawai (Kifune, 1984), comb. nov.; Sphecixenoslaetum (Ogloblin, 1926), comb. nov.; Sphecixenosorientalis (Kifune, 1985), comb. nov.; Sphecixenosreticulatus (Luna de Carvalho, 1972), comb. nov.; Sphecixenossimplex (Székessy, 1956), comb. nov.; Sphecixenosvanderiisti (Pasteels, 1952), comb. nov.; Tuberoxenosaltozambeziensis (Luna de Carvalho, 1959), comb. nov.; Tuberoxenossinuatus (Pasteels, 1956), comb. nov.; Tuberoxenossphecidarum (Siebold, 1839), comb. nov.; Tuberoxenosteres (Pasteels, 1950), comb. nov.; Tuberoxenostibetanus (Yang, 1981), comb. nov.; Deltoxenosbequaerti (Luna de Carvalho, 1956), comb. nov.; Deltoxenosbidentatus (Pasteels, 1950), comb. nov.; Deltoxenoshirokoae (Kifune & Yamane, 1992), comb. nov.; Deltoxenosiwatai (Esaki, 1931), comb. nov.; Deltoxenoslusitanicus (Luna de Carvalho, 1960), comb. nov.; Deltoxenosminor (Kifune & Maeta, 1978), comb. nov.; Deltoxenosrueppelli (Kinzelbach, 1971a), comb. nov.; Xenosropalidiae (Kinzelbach, 1975), comb. nov. Xenosminor Kinzelbach, 1971a, syn. nov. is recognized as a junior synonym of X.vesparum Rossi, 1793. Ophthalmochlusduryi Pierce, 1908, nomen nudum and Eupathoceralugubris Pierce, 1908, nomen nudum are recognized as nomina nuda and therefore unavailable in zoological nomenclature. The species diversity of Xenidae probably remains poorly known: the expected number of species is at least twice as high as the number presently described.

Frozen Antarctic path for dispersal initiated parallel host-parasite evolution on different continents.

After the break-up of Gondwana dispersal of organisms between America, Australia and Africa became more complicated. One of the possible remaining paths led through Antarctica, that was not yet glaciated and it remained habitable for many organisms. This favourable climate made Antarctica an important migration corridor for organisms with good dispersal ability, such as Aculeata (Hymenoptera), till the Oligocene cooling. Here we tested how cooling of Antarctica impacted global dispersal of Aculeata parasites (Strepsiptera: Xenidae). Our data set comprising six nuclear genes from a broad sample of Xenidae. Bayesian dating was used to estimate divergence times in phylogenetic reconstruction. Biogeography was investigated using event-based analytical methods: likelihood-based dispersal-extinction-cladogenesis and Bayesian models. The Bayesian model was used for reconstruction of ancestral host groups. Biogeographical methods indicate that multiple lineages were exchanged between the New World and the Old World + Australia until the Antarctica became completely frozen over. During the late Paleogene and Neogene periods, several lineages spread from the Afrotropics to other Old World regions and Australia. The original hosts of Xenidae were most likely social wasps. Within one lineage of solitary wasp parasites, parallel switch to digger wasps (Sphecidae) occurred independently in the New World and Old World regions. The biogeography and macroevolutionary history of Xenidae can be explained by the combination of dispersal, lineage extinction and climatic changes during the Cenozoic era. A habitable Antarctica and the presence of now-submerged islands and plateaus that acted as a connection between the New World and Old World + Australia provided the possibility for biotic exchanges of parasites along with their hymenopteran hosts. Although Xenidae are generally host specialists, there were significant host switches to unrelated but ecologically similar hosts during their evolution. There is little or no evidence for cophylogeny between strepsipteran parasites and hymenopteran lineages.