Hemipteran Diversity Through the Genomic Lens
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Original citation: Panfilio, Kristen A. and Angelini, David R.. (2018) By land, air, and sea : hemipteran diversity through the genomic lens. Current Opinion in Insect Science, 25 . pp. 106-115. Permanent WRAP URL: http://wrap.warwick.ac.uk/99196 Copyright and reuse: The Warwick Research Archive Portal (WRAP) makes this work of researchers of the University of Warwick available open access under the following conditions. This article is made available under the Creative Commons Attribution 4.0 International license (CC BY 4.0) and may be reused according to the conditions of the license. For more details see: http://creativecommons.org/licenses/by/4.0/ A note on versions: The version presented in WRAP is the published version, or, version of record, and may be cited as it appears here. For more information, please contact the WRAP Team at: [email protected] warwick.ac.uk/lib-publications Available online at www.sciencedirect.com ScienceDirect By land, air, and sea: hemipteran diversity through the genomic lens 1,2 3 Kristen A Panfilio and David R Angelini Thanks to a recent spate of sequencing projects, the Hemiptera representatives of the lice (Psocodea, [2]) and thrips are the first hemimetabolous insect order to achieve a critical (Thysanoptera, i5K project: GCA_000697945.1), form mass of species with sequenced genomes, establishing the the Paraneoptera. This superorder is also known as Acer- basis for comparative genomics of the bugs. However, as the caria and is traditionally considered the sister group clade most speciose hemimetabolous order, there is still a vast to the Holometabola [3,4]. With phylogenetically- swathe of the hemipteran phylogeny that awaits genomic informed surveys already suggesting that the Hemiptera representation across subterranean, terrestrial, and aquatic may serve as suitable outgroups to the Holometabola for a habitats, and with lineage-specific and developmentally plastic range of embryonic features [5,6], there is much to explore cases of both wing polyphenisms and flightlessness. In this in this order that can inform larger patterns of develop- review, we highlight opportunities for taxonomic sampling ment and evolution in the insects. beyond obvious pest species candidates, motivated by The Polyneoptera form the other major clade of hemime- intriguing biological features of certain groups as well as the tabolous insects [4]. Published genome assemblies for this rich research tradition of ecological, physiological, group include the large, repeat-heavy genome of the developmental, and particularly cytogenetic investigation that locust (Orthoptera, [7]). Investigations on eusociality spans the diversity of the Hemiptera. within the Dictyoptera — independent from a later origin of eusociality within the holometabolous Hymenop- Addresses 1 tera — have compared the genomes of termites relative School of Life Sciences, University of Warwick, Coventry CV4 7AL, to the cockroach [8–10]. In this fast-moving field, there is United Kingdom 2 Institute of Zoology: Developmental Biology, University of Cologne, even a recent first look at genomes of species among the 50674 Cologne, Germany ‘old wing’ orders Odonata and Ephemeroptera [11 ], out- 3 Department of Biology, Colby College, Waterville, ME 04901, groups to the Neoptera. Meanwhile, the Hemiptera cur- United States rently comprise over half of the hemimetabolous species Corresponding author: Panfilio, Kristen A (Kristen.Panfilio@alum. with sequenced genomes listed on the central insect swarthmore.edu) genomics GitHub portal (as of October 2017, http://i5k. github.io/arthropod_genomes_at_ncbi). Current Opinion in Insect Science 2018, 25:xx–yy Hemipterans have diversified into a variety of habitats This review comes from a themed issue on Insect genomics where they make use of a range of food sources. Some Edited by Stephen Richards, Anna Childers, and Christopher members, such as aphids and planthoppers, have become Childers notorious agricultural pests, while the evolutionary history of the group has been characterized by numerous shifts between predation and plant feeding [12]. Underlying these specializations is the defining feature of the Hemi- https://doi.org/10.1016/j.cois.2017.12.005 ptera: a common anatomy of piercing-sucking mouthparts 2214-5745/ã 2017 The Authors. Published by Elsevier Inc. This is an (Figure 1a). Indeed, investigation of mouthpart develop- open access article under the CC BY license (http://creativecommons. ment in the milkweed bug Oncopeltus fasciatus represents org/licenses/by/4.0/). one of the earliest functional studies using RNA interfer- ence (RNAi) in the insects [13]. O. fasciatus has a long and active research tradition in developmental biology, genet- The Hemiptera: feeding, functional genetics, ics, and other fields, which has led to the recent sequenc- and hemimetabolous diversity ing and comparative analysis of its genome ([14 ], and see With an estimated 82,000 described species, roughly 9% of below). In general, RNAi is highly effective in the Het- all known insects belong to the Hemiptera [1], making the eroptera (‘true bugs’), with several species maintained as bugs the fifth largest insect order after the holometabolous laboratory research models (Figure 1b, [13,15–18,19 ]). In flies, butterflies, beetles, and ants. In contrast to those contrast, to date there has been mixed success in using other four orders, the Hemiptera belong to the hemime- RNAi on mucivorous (sap feeding) agricultural pests of the tabolous insect radiation, a part of the insect family tree Sternorrhyncha, both for environmental delivery and for that retains many ancestral insect states that are just systemic efficacy [20,21]. However, genetically and phe- beginning to be investigated in the current genomics notypically detectable knockdown can be obtained with era. The Hemiptera, along with recently sequenced particularly high dsRNA concentrations via feeding or Current Opinion in Insect Science 2018, 25:106–115 www.sciencedirect.com Hemipteran diversity through the genomic lens Panfilio and Angelini 107 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. In 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. injection, with discretionary ‘boost’ secondary injections, behaviors. Although most eukaryotes are typified by in the pea aphid [22,23]. monocentric chromosomes, many lineages feature holo- centric chromosomes in which spindle microtubules con- Here, we survey the hemipteran species that have been nect at many points along the chromosome without a sequenced, looking at their value beyond their immediate distinct kinetochore. This mode of cell division is seen in sequencing justifications, and thereby establish the basis for an estimated 16% of insect species [24], including the our selection of future sequencing projects, sampling taxa Odonata, Dermaptera, Psocodea, Lepidoptera, Trichop- from habitats as diverse as the land, air, and sea (Figure 2). tera, and Hemiptera, as well as in other arthropods such as some arachnids [25]. Holocentric chromosomes continue Holocentric chromosomes and karyotype to segregate normally even when fragmented, perhaps evolution explaining the resistance of species like O. fasciatus to In the mid-twentieth century, cytogenetics explored the mutation from ionizing radiation [26]. One prediction of diversity of chromosome structures and meiotic the persistence of chromosomal fragments may be an www.sciencedirect.com Current Opinion in Insect Science 2018, 25:106–115 108 Insect genomics 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