COIS 408 1–10 Available online at www.sciencedirect.com ScienceDirect 1 2 By land, air, and sea: hemipteran diversity through the 3 genomic lens 1,2 3 4Q1 Kristen A Panfilio and David R Angelini 5 Thanks to a recent spate of sequencing projects, the Hemiptera form the Paraneoptera. This superorder is also known 45 6 are the first hemimetabolous insect order to achieve a critical as Acercaria and is traditionally considered the sister 46 7 mass of species with sequenced genomes, establishing the group clade to the Holometabola [3,4]. With phylogenet- 47 8 basis for comparative genomics of the bugs. However, as the ically-informed surveys already suggesting that the 48 9 most speciose hemimetabolous order, there is still a vast Hemiptera may be suitable outgroups to the Holometa- 49 10 swathe of the hemipteran phylogeny that awaits genomic bola for a range of embryonic features [5,6], there is much 50 11 representation across subterranean, terrestrial, and aquatic to explore in this order that can inform larger patterns of 51 12 habitats, and with lineage-specific and developmentally plastic development and evolution in the insects. 52 13 cases of both wing polyphenisms and flightlessness. In this 14 review, we highlight opportunities for taxonomic sampling The Polyneoptera form the other major clade of hemi- 53 15 beyond obvious pest species candidates, motivated by metabolous insects [4]. Published genome assemblies for 54 16 intriguing biological features of certain groups as well as the this group include the large, repeat-heavy genome of the 55 17 rich research tradition of ecological, physiological, locust (Orthoptera) [7]. Investigations on eusociality 56 18 developmental, and particularly cytogenetic investigation that within the Dictyoptera — independent from a later origin 57 19 spans the diversity of the Hemiptera. of eusociality within the holometabolous Hymenoptera — 58 have compared the genomes of termites relative to the 59 Addresses cockroach [8–10]. In this fast-moving field, there is even a 60 20 1 School of Life Sciences, University of Warwick, Coventry CV4 7AL, recent first look at genomes of species among the ‘old 61 21 United Kingdom 62 22 2 wing’ orders Odonata and Ephemeroptera [11 ], outgroups Institute of Zoology: Developmental Biology, University of Cologne, 23 63 50674 Cologne, Germany to the Neoptera. Meanwhile, the Hemiptera currently 24 3 Department of Biology, Colby College, Waterville, ME 04901, United comprise over half of the hemimetabolous species with 64 25 States sequenced genomes listed on the central insect genomics 65 GitHub portal (as of October 2017, http://i5k.github.io/ 66 Corresponding author: Panfilio, Kristen A (Kristen.Panfilio@alum. 67 swarthmore.edu) arthropod_genomes_at_ncbi). Hemipterans have diversified into a variety of habitats 68 26 Current Opinion in Insect Science 2018, 25:xx–yy where they make use of a range of food sources. Some 69 27 This review comes from a themed issue on Insect genomics members, such as aphids and planthoppers, have become 70 28 Edited by Stephen Richards, Anna Childers, and Christopher notorious agricultural pests, while the evolutionary his- 71 29 Childers tory of the group has been characterized by numerous 72 shifts between predation and plant feeding [12]. Under- 73 lying these specializations is the defining feature of the 74 Hemiptera: a common anatomy of piercing-sucking 75 30 doi:10.1016/j.cois.2017.12.005 mouthparts (Figure 1a). Indeed, investigation of mouth- 76 31 2214-5745/ã 2017 The Authors. Published by Elsevier Inc. part development in the milkweed bug Oncopeltus fas- 77 ciatus represents one of the earliest functional studies using RNA interference (RNAi) in the insects [13]. 78 32 The Hemiptera: feeding, functional genetics, O. fasciatus has a long and active research tradition in 79 33 and hemimetabolous diversity developmental biology, genetics, and other fields, which 80 34 With an estimated 82 000 described species, roughly 9% had led to the recent sequencing and comparative anal- 81 35 of all known insects belong to the Hemiptera [1], making ysis of its genome ([14 ], and see below). In general, 82 36 the bugs the fifth most diverse insect order after the RNAi is highly effective in the Heteroptera (‘true 83 37 holometabolous flies, butterflies, beetles, and ants. By bugs’), with several species maintained as laboratory 84 38 contrast to those other four orders, the Hemiptera belong research models (Figure 1b, [13,15–18,19 ]). By con- 85 39 to the hemimetabolous insect radiation, a part of the trast, to date there has been mixed success in using 86 40 insect family tree that retains many ancestral insect RNAi on mucivorous (sap feeding) agricultural pests of 87 41 states that are just beginning to be investigated in the the Sternorrhyncha, both for environmental delivery and 88 42 current genomics era. The Hemiptera, along with recently for systemic efficacy [20,21]. However, genetically and 89 43 sequenced representatives of the lice (Psocodea, [2]) and phenotypically detectable knockdown can be obtained 90 44 thrips (Thysanoptera; i5K project: GCA_000697945.1), with particularly high dsRNA concentrations via feeding www.sciencedirect.com Current Opinion in Insect Science 2017, 25:1–10 Please cite this article in press as: Panfilio KA, Angelini DR: By land, air, and sea: hemipteran diversity through the genomic lens, Curr Opin Insect Sci (2017), https://doi.org/10.1016/j. cois.2017.12.005 COIS 408 1–10 2 Insect genomics Figure 1 (a) Hemipteran mouthpart anatomy mandibular stylets maxillary stylets labium salivary pump salivary gland clypeus food salivary muscle stylets canal canal labrum dorsal anterior view rostrum in cross section stylets in cross section (b) Experimental tractability (RNAi) WT Jhae-DIIRNAi Current Opinion in Insect Science Bugs suck: unique mouthpart anatomy underlies diverse feeding ecologies in the Hemiptera and highlights their experimental tractability. (a) All Hemiptera are characterized by conserved piercing-sucking mouthpart anatomy comprised of the labium, which acts as the outer support scaffold, and retractable, piercing stylets. These mouthparts can be deployed for feeding on a variety of fluid and solid substrates from diverse plants and animals (adapted from [24,101]). (b) The Heteroptera (‘true bugs’) are particularly amenable to functional molecular genetics techniques such as parental RNAi, here exemplified by knockdown of the Distal-less orthologue in the soapberry bug, Jadera haematoloma. By contrast with a wild type hatchling (WT, left), all appendages in a knockdown individual are severely truncated (right). This includes the labium (delimited by horizontal blue bars), such that the translucent stylets protrude substantially and are not supported (dashed blue line). Hatchlings (first instar nymphs) are shown in ventral aspect; scale bars are 200 mm. 91 or injection, with discretionary ‘boost’ secondary injec- behaviors. Although most eukaryotes are typified by 102 92 tions, in the pea aphid [22,23]. monocentric chromosomes, many lineages feature holo- 103 centric chromosomes in which spindle microtubules con- 104 93 Here, we survey the hemipteran species that have been nect at many points along the chromosome without a 105 94 sequenced, looking at their value beyond their immediate distinct kinetochore. This mode of cell division is seen in 106 95 sequencing justifications, and thereby establish the basis for an estimated 16% of insect species [24], including the 107 96 our selection of future sequencing projects, sampling taxa Odonata, Dermaptera, Psocodea, Lepidoptera, Trichop- 108 97 from habitats as diverse as the land, air, and sea (Figure 2). tera, and Hemiptera, as well as in other arthropods such as 109 some arachnids [25]. Holocentric chromosomes continue 110 98 Holocentric chromosomes and karyotype to segregate normally even when fragmented, perhaps 111 99 evolution explaining the resistance of species like O. fasciatus to 112 100 In the mid-twentieth century, cytogenetics explored mutation from ionizing radiation [26]. One prediction of 113 101 the diversity of chromosome structures and meiotic the persistence of chromosomal fragments may be an 114 Current Opinion in Insect Science 2017, 25:1–10 www.sciencedirect.com Please cite this article in press as: Panfilio KA, Angelini DR: By land, air, and sea: hemipteran diversity through the genomic lens, Curr Opin Insect Sci (2017), https://doi.org/10.1016/j. cois.2017.12.005 COIS 408 1–10 Hemipteran diversity through the genomic lens Panfilio and Angelini 3 Figure 2 Hemiptera Species Feeding Pest Notes Genome sequence? Selected (291 mya) ecology level transcriptomes Acyrthosiphon pisum mucivory: ++ Crop pest; Phenotypic plasticity [32] [106] (pea aphid) legumes and host-endosymbiont studies various aphids (Aphididae: mucivory: e.g., ++ Diverse family (>4,000 species); [33] *a; [34] *a; [35] Myzus persicae, Aphis peach, soybean, many crop pests glycines, Diuraphis noxia) wheat Mealybugs (Pseudococcidae): mucivory: + Subtropical pest; its “manna” [46, 47] Six species from six genera cotton, papaya honeydew is harvested by ants Bemisia tabaci cryptic species mucivory: e.g., ++ Crop pest; globally invasive; [36] *i complex (silverleaf whitefly) cassava, tomato vector of numerous plant viruses Pachypsylla venusta mucivory: + Crop pest i5K: [37] *i (hackberry petiole gall psyllid) hackberry Sternorrhyncha Diaphorina citri mucivory: ++ Crop pest; globally invasive; [38] *i (Asian citrus psyllid) citrus plants vector of numerous plant viruses 13-