Fossils reshape the Sternorrhyncha evolutionary tree (Insecta, Hemiptera)

www.nature.com/scientificreports OPEN Fossils reshape the Sternorrhyncha evolutionary tree (Insecta, Hemiptera) Jowita Drohojowska Patrick Müller5,6 1* , Jacek Szwedo 2* , Dagmara Żyła 2,3 , Di‑Ying Huang4 & The Sternorrhyncha, which comprise about 18,700 described recent species, is a suborder of the Hemiptera, one of big five most diverse insect orders. In the modern fauna, these tiny phytophages comprise insects of great ecological and economic importance, like aphids (Aphidomorpha), scale insects (Coccidomorpha), whiteflies (Aleyrodomorpha) and psyllids (Psylloidea). Their evolutionary history can be traced back to the Late Carboniferous, but the early stages of their evolution and diversification is poorly understood, with two known extinct groups—Pincombeomorpha and Naibiomorpha variously placed in classifications and relationships hypotheses. Most of the recent Sternorrhyncha groups radiated rapidly during the Cretaceous. Here we report the new finding of very specialised sternorrhynchans found as inclusions in mid-Cretaceous amber from Kachin state (northern Myanmar), which represent another extinct lineage within this hemipteran suborder. These fossils, proposed to be placed in a new infraorder, are revealed to be related to whiteflies and psyllids. We present, also for the first time, the results of phylogenetic analyses covering extinct and extant lineages of the Sternorrhyncha. The Hemiptera is an ancient insect order, demonstrating extraordinary life histories and highly specialized morphological adaptations, as they have exploited diverse habitats and food sources through over 300 million years of their evolution. Hemiptera is one of the Big Five insect orders (with Coleoptera, Diptera, Lepidoptera and Hymenoptera), the most diversified and speciose orders among all insects, the largest non-holometabolous order of insects, representing approximately 7% of metazoan diversity. The Hemiptera currently contains around 320 extant and extinct families, which is the highest number among all insect orders1, with over 110,000 species already described2–4. The order Hemiptera is subdivided into six suborders1—extinct Paleorrhyncha (archescytinoids), Sternorrhyncha (modern aphids, scale insects, whiteflies, jumping plantlice, and their extinct relatives), Fulgoromorpha (planthoppers), Cicadomorpha (cicadas, froghoppers, leafhoppers, treehoppers, and number of extinct groups), Coleorrhyncha (moss bugs) and Heteroptera (true bugs). Representatives of the Sternorrhyncha are tiny sucking phytophagous insects, representing nearly 19,000 described extant and extinct species distributed worldwide. They are highly diverse morphologically and ecologically, containing several extant infraorders Aphidomorpha, Coccidomorpha, Aleyrodomorpha) and Psyllodea, as well as extinct ones Naibiomorpha and P incombeomorpha1,4. Both the fossil record from Moscovian of A vion5 6 and molecular divergence e stimation show that the group was present during the Carboniferous. Sternorrhyncha have been evolving and diversifying for over 300 million years, but their fossils are less numerous than fossils of euhemipteran lineages (Fulgoromorpha, Cicadomorpha, Coleorrhyncha, and Heteroptera). 1 Institute of Biology, Biotechnology and Environmental Protection, University of Silesia, 9, Bankowa St., 40‑007 Katowice, Poland. 2Laboratory of Evolutionary Entomology and Museum of Amber Inclusions, Department of Invertebrate Zoology and Parasitology, University of Gdańsk, 59, Wita Stwosza St., 80‑308 Gdańsk, Poland. 3Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, USA. 4State Key Laboratory of Palaeobiology and Stratigraphy, Center for Excellence in Life and Paleoenvironment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China. 5Kaeshofen, Germany. 6Amber Study Group, c/o Geological-Palaeontological Museum of the University of Hamburg, Bundesstraße 55, 20146 Hamburg, Germany. *email: ; jacek.szwedo@ biol.ug.edu.pl Scientific Reports | (2020) 10:11390 | https://doi.org/10.1038/s41598-020-68220-x 1 Vol.:(0123456789) www.nature.com/scientificreports/ Figure 1.  Phylogenetic position of Dingla shagria gen. sp. nov. on most parsimonius tree. Numbers at nodes represent posterior probabilities and bootstrap values. Image of planthopper Pyrops candelaria: Max Pixel Public Domain CC0 (modified); pincombeid Pincombea sp. redrawn from46; male scale insect: Pavel Kirillov CC-BY-SA2.0 (modified); Coccavus supercubitus redrawn from46; aphid Macrosiphum rosae: Karl 432 CC-BY-SA4.0 (modified); protopsyllidiid Poljanka hirsuta redrawn from47; liadopsyllid Liadopsylla apedetica redrawn from48; whitefly Aleyrodes proletella: Amada44 CC-BY-SA4.0 (modified); psyllid Trioza urticae photo by Jowita Drohojowska. The consensus is that the Sternorrhyncha are a monophyletic lineage, but their internal classification is still an object of debate. Their sedentary lifestyles coupled with phloem-feeding behaviours in these insects, which behave as plant parasites, have driven morphological reductions and losses, neotenous females, extreme sexual dimorphism, and convergently derived morphological characters that would otherwise be useful in phylogenetic analyses. Thus, reconstructing the relationships of Sternorrhyncha is rather challenging. While Aphidomorpha and Coccidomorpha seem to be closely related, the placement of Naibiomorpha remains disputed. This group was placed within Aphidomorpha8 or in Coccidomorpha9. The Pincombeomorpha seems to form a distinct lineage together with Aphidiformes (i.e. Aphidomorpha + Naibiomorpha + Coccidomorpha). The second clade of Sternorrhycha—Psylliformes contains Aleyrodomorpha with Aleyrodidae and Psylloidea, the latter recently united with Protopsyllidioidea as P syllodea1. Grimaldi10 stated that Protopsyllidiidae, which was once placed in 11 Pincombeoidea , should be placed as a sister group of all remaining Sternorrhyncha. However, in that analysis, representatives of the other extinct sternorrhynchan groups such as Pincombeomorpha and Naibioidea (Naibiomorpha) were not included. As a result of all these proposals, Psyllodea, as recently r ecognised1, seems to be a paraphyletic group and Protopsyllidiidae are not deemed to be direct ancestors of P sylloidea12. Recently, the morphological features, taxonomic content and classification of Protopsyllidioidea were reanalysed and a new hypothesis of their relationships was proposed, with Protopsyllidiidae as sister group to the Psylloidea + Aleyrodoidea clade13. Drohojowska14 postulated that Liadopsyllidae could be a sister group to the Psylloidea + Aleyrodoidea clade, based on morphological analysis of extant and extinct taxa. The fossils described below are so morphologically remote and disparate from the other extinct and extant groups, that they cannot be placed in any of already proposed groups. They can be recognised as sternorrhyncha (...truncated)