Hemipteran Diversity Through the Genomic Lens, Curr Opin Insect Sci (2017)

COIS 408 1–10

Available online at www.sciencedirect.com ScienceDirect

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

are the ﬁrst hemimetabolous insect order to achieve a critical as Acercaria and is traditionally considered the sister 46

mass of species with sequenced genomes, establishing the group clade to the Holometabola [3,4]. With phylogenet- 47

basis for comparative genomics of the bugs. However, as the ically-informed surveys already suggesting that the 48

most speciose hemimetabolous order, there is still a vast Hemiptera may be suitable outgroups to the Holometa- 49

swathe of the hemipteran phylogeny that awaits genomic bola for a range of embryonic features [5,6], there is much 50

representation across subterranean, terrestrial, and aquatic to explore in this order that can inform larger patterns of 51

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

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

Current Opinion in Insect Science 2018, 25:xx–yy

where they make use of a range of food sources. Some 69

This review comes from a themed issue on Insect genomics

members, such as aphids and planthoppers, have become 70

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

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

33 and hemimetabolous diversity developmental biology, genetics, and other ﬁelds, which

34 With an estimated 82 000 described species, roughly 9% had led to the recent sequencing and comparative anal-

35 of all known insects belong to the Hemiptera [1], making ysis of its genome ([14 ], and see below). In general,

36 the bugs the ﬁfth most diverse insect order after the RNAi is highly effective in the Heteroptera (‘true

37 holometabolous ﬂies, butterﬂies, beetles, and ants. By bugs’), with several species maintained as laboratory

38 contrast to those other four orders, the Hemiptera belong research models (Figure 1b, [13,15–18,19 ]). By con-

39 to the hemimetabolous insect radiation, a part of the trast, to date there has been mixed success in using

40 insect family tree that retains many ancestral insect RNAi on mucivorous (sap feeding) agricultural pests of

41 states that are just beginning to be investigated in the the Sternorrhyncha, both for environmental delivery and

42 current genomics era. The Hemiptera, along with recently for systemic efﬁcacy [20,21]. However, genetically and

43 sequenced representatives of the lice (Psocodea, [2]) and phenotypically detectable knockdown can be obtained

44 thrips (Thysanoptera; i5K project: GCA_000697945.1), with particularly high dsRNA concentrations via feeding

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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

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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- and 17-year periodical mucivory: + Longevity and timing of life cycle; Needed, e.g., ERX050785 cicadas (e.g., Magicicada tree root xylem hybridization and speciation; PRJNA203146 ** septendecim) climate change adaptation Homalodisca vitripennis mucivory: + Crop pest i5K: [107] (glassy-winged sharpshooter) generalist GCA_000696855.1 *i (grapes, citrus) Treehoppers (Membracidae; phytophagy: + Unique pronotal helmet; highly Needed 1KITE: e.g., Centrotus cornutus, flowering plants; diverse (>3,200 species) PRJNA272169, Campylenchia latipes) grasses PRJNA272226 Moss bugs (Peloridiidae; e.g., phytophagy: - Unique morphology; single extant Needed 1KITE: [4], Xenophysella greensladeae, moss family of a Gondwanan relict PRJNA272276 Auchenorrhyncha Peloridium pomponorum) insect lineage, good fossil record Lanternflies (Fulgoridae; e.g., phytophagy: + Unique head structures; highly Needed, e.g., L. delicatula: Zanna intricata, Lycorma flowering plants; diverse (>700 species) e.g., Z. intricata: PRJNA357415 delicatula) grasses PRJNA338883 ***

Planthoppers (Delphacidae): mucivory: ++ Serious pests of rice; N. lugens [50-52] [108] Three species of three genera rice wing polyphenism studies Gerris buenoi carnivory: - Developmental and biomechanical i5K: [64] *i: (water strider) insects studies, aquatic adaptation (RNAi) GCA_001010745.1

Halobates micans carnivory: - Lives on the open ocean: salinity Needed (sea skater) plankton tolerance and dispersal research; distributed across the tropics Giant water bugs carnivory: - Unique salivary enzymes; parental Needed 1KITE: (Belostomatidae; e.g., aquatic care; neglected taxon PRJNA272220 Belostoma ﬂumineum) invertebrates Shore bugs (Saldidae; carnivory: - Sister taxon to Cimicomorpha + Needed 1KITE: e.g., Saldula saltatoria) insects Pentatomomorpha PRJNA272204

Rhodnius prolixus hematophagy: ++ Vector of Chagas disease [71] *v [109, 110] (kissing bug) amniote infection in humans;

(156 mya) vertebrates Embryological studies (RNAi) Heteroptera Arilus cristatus carnivory: - Pronotal elaboration; Reduviidae Needed 1KITE: (wheel bug) insects are highly diverse (7,000 species) PRJNA272219 Cimex lectularius hematophagy: ++ Global human ectoparasite with i5K: [72] *i *v; [73] [111] (bed bug) mammals and increasing insecticide resistance birds

Lygus lineolaris, L. hesperus mucivory / ++ Crop pests; represents the diverse Needed [74, 75] (tarnished plant bugs) phytophagy: Miridae (>11,000 species)

Cimicomorpha cotton, alfalfa

Jadera haematoloma phytophagy: - Evolutionary ecology studies Needed (soapberry bug) soapberry family (RNAi: see Fig. 1) Riptortus pedestris phytophagy: ++ Crop pest Needed [112] (bean bug) beans Leptoglossus occidentalis phytophagy: + Representative of the leaf-footed Needed (western conifer seed bug) pines bugs (~1,900 species); invasive

Pyrrhocoris apterus phytophagy: - Endocrinology (RNAi) and Needed PRJNA171139, (red ﬁrebug) Malvales chronobiology studies, early PRJNA272203 (mallow, lime, model for karyotyping and (1KITE), linden) seeds cytogenetics PRJNA389968 Oncopeltus fasciatus phytophagy: - Physiology and developmental i5K: [14] *i [113, 114] (milkweed bug) milkweed seeds studies (RNAi) Halyomorpha halys phytophagy: ++ Crop pest; invasive population i5K: [115, 116] Pentatomomorpha (brown marmorated stink bug) generalist dynamics GCA_000696795.1 *i

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4 Insect genomics

115 elevated evolutionary rate of rearrangement, with some identify lineage-speciﬁc factors that regulate holocentric 154

116 holocentric lineages prone to rapid karyotype evolution. mitosis and meiosis. 155

117 As one afﬁrmative example, the peach potato aphid

118

undergoes rapid rearrangements, allowing selection for Taxonomic survey of available and needed 156

119

insecticide resistance [27]. hemipteran genomes 157

Many species of Sternorrhyncha (aphids, psyllids, white- 158

120

Genomic insights from the Hemiptera and other insect ﬂies) are serious agricultural pests. Therefore, they have 159

121

groups suggest fundamental differences in the evolution received understandable research attention and remain 160

122

of holocentrism among different lineages [28 ]. The cell prominent candidates for genome sequencing [32–38]. 161

123

biology of holocentric cell division has been studied in Here, we focus on the larger diversity of the Hemiptera 162

124

detail in the nematode Caenorhabditis elegans, where the (Figure 2), a fascinating insect order that has a substantial 163

125

centromeric histone H3 variant CenH3 is required for basic research tradition extending over 100 years. 164

126

mitosis. By contrast, all holocentric insect species lack Although two-thirds of currently sequenced hemipterans 165

127

CenH3 as well as the inner kinetochore protein CenpC are high-status pests, most of the taxa we propose for 166

128

[28 ], and it remains unclear how diverse the mecha- future genome sequencing are rather justiﬁed by their use 167

129

nisms for kinetochore assembly and cell division may be in basic research or by their unique biology. 168

130 in holocentric insects. There may also be genome struc-

131

tural differences, such as an absence or redistribution of Moreover, there is more to pest species’ biology than their 169

132

the ﬁxed length repetitive sequences that typify centro- status as pests. Such species are effective at exploiting 170

133

meric DNA in monocentric species such as Drosophila agricultural plant food sources in part because of under- 171

melanogaster [29]. lying biological features such as developmental plasticity 172

and microbial symbioses. For example, wing polyphen- 173

134

The Hemiptera possess a remarkable diversity of mei- isms that underlie migratory behavior have been geneti- 174

135

otic processes, including apomictic parthenogenesis, cally dissected by global and candidate gene approaches 175

136

non-chiasmatic segregation, and inverted meiosis [25]. in species such as the pea aphid [23,39] and the brown 176

137

The study of these poorly understood phenomena may planthopper, Nilaparvata lugens (a member of the Auche- 177

138

provide fundamental insights into cell division. For norrhyncha whose wing polymorphism is also reviewed 178

139

example, holocentric chromosomes are often associated in this issue [40]). Meanwhile, given the low-nutrient diet 179

140

with inverted meiosis, in which the common order of of mucivores, sequencing of the hemipteran host has 180

141

reductional and equational cell divisions is reversed [30]. frequently garnered additional data for genomes of their 181

142

Although all Hemiptera possess holocentric chromo- bacterial endosymbionts. These microorganisms geneti- 182

143

somes, inverted meiosis is known only from some cally and nutritionally complement the insects’ physiol- 183

144

groups, such as the soft scale insects (Coccidae), while ogy, enabling them to exploit host plants (e.g., [41–45]). 184

145

others like the Heteroptera maintain the traditional Within the Sternorrhyncha, mealybugs, or scale insects, 185

146

meiotic order [30]. A better understanding of these feature the intriguing situation of tripartite, nested sym- 186

147

diverse meiotic mechanisms may have relevance beyond bioses wherein the insects’ bacterial symbionts them- 187

148

insects, since non-canonical patterns of meiotic division, selves have intrabacterial symbionts. Recent study of 188

149

similar to inverted meiosis, have been inferred from gene complementation and symbiont evolutionary histo- 189

150

SNP segregation in human oocytes [31]. Below, we ries has led to draft genome assemblies for six mealybug 190

151

highlight some of the extensive cytogenetic work that species and their bacterial constituents [46 ,47]. These 191

152

has been done in the Hemiptera, which will literally genomic resources also provide a foundation for future 192

153

scaffold future genome sequencing efforts as well as exploration of other biological features in these species. 193

(Figure 2 Legend) Hemiptera with sequenced genomes and those that would strongly augment biological and taxonomic diversity for comparative

genomics. Most species sequenced to date are primarily agricultural pests and disease vectors. For many of the needed taxa, a wealth of

transcriptomic data are already available, such as through the 1KITE initiative (e.g., [4]), while a pilot project of the i5K initiative [102] has made

good headway in generating a critical mass of sequenced species for this most species-rich hemimetabolous insect order (e.g., [14 ,37,64,72],

and listed project accessions). Species suggested here for sequencing would then cover the major families of the Hemiptera and span a wide

range of anatomical features (e.g., pronotal and head elaborations) and ecological niches (subterranean, aquatic, carnivorous). Furthermore,

suggested species such as Jadera haematoloma and Pyrrhocoris apterus represent particularly tractable laboratory research models (e.g.,

Figure 1b). Phylogenetic relationships are primarily based on [62 ], with further support for infraorder resolution for the Sternorrhyncha [103,104]

and Cimicomorpha [61]. However, hemipteran relationships remain contested, in part reflected by dashed lines in the dendrogram. The

Cimicomorpha have traditionally been recovered as a monophyletic clade with various internal topologies [24,61,77,105]. However, recent

mitochondrial phylogenomic data — although problematic [79] — suggest that this infraorder may be paraphyletic with respect to the

Pentatomomorpha [62 ]. Furthermore, the position of Pyrrhocoris apterus within the Pentatomomorpha is unstable even across studies using

comparable mitochondrial datasets (cf., [62 ] vs. [78]). Divergence times are the median values reported in [4]. Accession numbers refer to

projects in GenBank. Asterisks in the table indicate current sequence statuses, as of November 2017: (*) publically accessible, BLASTable genome

browser hosted by AphidBase (*a: http://bipaa.genouest.org/is/aphidbase/), i5K (*i: https://i5k.nal.usda.gov/), and/or VectorBase (*v: https://www.

vectorbase.org); (**) no public data yet available; (***) unassembled, raw data thus far (SRA).

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Hemipteran diversity through the genomic lens Panfilio and Angelini 5

194 As one example, mealybugs exhibit extreme sexual Auchenorrhyncha that would beneﬁt from genomic inves- 249

195 dimorphism, with ﬂightless females and an unusual form tigation of their distinctive cuticular projections from the 250

196 of sex determination. Males may arise from unfertilized pronotum and head (Figure 2; e.g., [60]). 251

197 eggs or via differential epigenomic regulation that leads to

198 the unusual process of heterochromatization and elimi- Many Hemiptera belong to the clade of ‘true bugs’, the 252

199 nation of the paternal genome [48,49]. Heteroptera. Relationships in this group remain uncer- 253

tain, but the base of this radiation appears to be a para- 254

200 The Auchenorrhyncha (cicadas, treehoppers, moss bugs) phyletic assemblage of aquatic Heteroptera, whose habi- 255

201 contain opportunities to investigate life cycle regulation tats range from ponds to the open ocean [61,62 ]. 256

202 and a range of lineage-speciﬁc anatomical elaborations Although aquatic insects are generally prone to fossiliza- 257

203 (Figure 2). Although genomes have recently been pub- tion, no stem group fossil Heteroptera have been found 258

204 lished for planthoppers as major pests of rice [50–52], from the Permian, when the group is thought to have 259

205 most Auchenorrhyncha have been sorely neglected. With diversiﬁed [24]. Additional genomic resources will clarify 260

206 over 1300 species, cicadas (Cicadidae) represent a fasci- the evolutionary origins and molecular basis of hetero- 261

207 nating group for investigation of biological rhythms, from pteran diversiﬁcation and aquatic adaptations. Within 262

208 loud nightly singing to rare, gregarious emergences. In the infraorder Gerromorpha, both tissue-speciﬁc and 263

209 particular, the periodical cicadas of the genus Magicicada species-speciﬁc transcriptomes have already supported 264

210 are among the longest lived insects, with a predominantly developmental genetics investigations of male antennal 265

211 subterranean life style that culminates in a brief sexual modiﬁcations for grasping the female during mating on 266

212 adulthood on the surface in cycles of 13 or 17 years. the water surface [63] and of the origin of the propelling 267

213 Phylogenetic investigations with DNA from a rich, his- leg fan used for locomotion in veliid species [19 ]. The 268

214 torical voucher collection revealed repeated, independent recently sequenced genome of the water strider Gerris 269

215 divergence to 13-year or 17-year cycles [53]. These buenoi (Figure 2, [64]) represents a key ﬁrst reference for

216 changes may reflect geologic climatic fluctuations and these taxa and should help identify other lineage-specific 270

217 environmental plasticity, rather than potential hybridiza- adaptations. For example, the fellow gerrid Halobates 271

218 tion among sympatric species, but the need for genomic- micans is the only insect capable of living entirely at

219 scale analyses has already been recognized [53,54 ]. The sea, on the ocean surface, where ecological challenges 272

220 requirements for cicadas’ underlying molecular clocks — include dispersal, water pollution, and tolerance to salt, 273

221 including both synchronization across populations and temperature, and UV exposure [65,66]. Genomic infor- 274

222 entrainment to the environment — provide a engaging mation for this species in comparison with that for the 275

223 challenge to unpick in terms of evolutionary lability, shore bugs (Saldidae), which dwell in the intertidal zone 276

224 current cellular function, and potential scope for future and face similar pressures [67], has the potential to reveal 277

225 adaptation to climate and habitat change [55]. Potential whether convergent molecular features underpin these 278

226 epigenomic regulation across the life cycle would be a key lineages’ independent adaptations to such environmental 279

227 feature for future investigation. For example, while it is conditions. 280

228 still early days, a range of epigenetic regulatory mecha-

229 nisms has been implicated in the commitment to solitary The giant water bugs (Belostomatidae) are a striking 281

230 or gregarious phases in swarming locusts (reviewed in taxon not only for their tremendous size, as the name 282

231 [56 ]). Although cicada genomes are large by insect Giganometra gigas implies [68], but also for their parental

232 standards (5–7 Gb), the wealth of SNP and RAD- care. Males brood eggs to ensure their exposure to air [12] 283

233 seq data already available for closely related individuals and deploy chemical defenses against potential predators 284

234 and species within the Magicicada [54 ] provides a strong such as ants [69]. ‘Heteroptera’ literally refers to the 285

235 foundation for comparative genomics, more akin to the mixed composition of bugs’ forewings, with both mem- 286

236 situation in mammals in terms of recent divergence branous and hardened regions (‘hemelytra’, [62 ]). Belas- 287

237 times and dense sampling. tomids have uniquely taken advantage of the hemelytra 288

to create air pockets that help them to stay aﬂoat, through 289

238 With their unique, ﬂightless morphology and rich fossil specialized abdominal modiﬁcations that channel air 290

239 record, moss bugs (Peloridiidae) are often described as [70]. Building on recent transcriptomic work (Figure 2), 291

240 living relicts from the Permian. The group is the subject genome sequencing within this family will open new 292

241 of a handful of anatomical studies pertaining to their avenues for research on respiratory physiology, chemical 293

242 specialized cuticular secretions and exoskeletal func- communication, and morphological innovation. 294

243 tional properties within damp, temperate climates (e.g.,

244 [57,58]). Recent transcriptome sequencing and karyotyp- Within the Cimicomorpha, genomes have been 295

245 ing (e.g., [4,59]) will support future genomic investigation sequenced for obligate blood-feeding human ectopara- 296

246 of this ancient, seemingly unchanging lineage. Similarly, sites: the bed bug and the kissing bug [71–73], which 297

247 transcriptomes are already available for treehoppers represent evolutionarily independent instances of hema- 298

248 (Membracidae) and lanternﬂies (Fulgoridae), fellow tophagy in the Cimicidae and Reduviidae, respectively 299

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6 Insect genomics

300 [62 ]. By contrast, with over 11 000 described species, across North America and become introduced in Europe, 351

301 genomic resources are greatly needed for the Miridae, a where it can be a destructive pest of conifer trees [87]. 352

302 large family of mostly plant-feeding bugs. To date, work Meanwhile, the crop pest Riptortus pedestris has emerged 353

303 has focused on the polyphagous tarnished plant bugs of as a new model to examine hemipteran-bacterial symbi- 354

304 the genus Lygus. Transcriptome analysis of these promi- osis [88,89]. As in the Mirini, work on these invasive 355

305 nent agricultural pests has explored how their salivary generalists can be contrasted with results from closely 356

306 gland products facilitate the external digestion of plant related phytophagous specialists. Many pentatomomor- 357

307 tissues [74] and the molecular basis of insecticide resis- phan specialists have achieved the metabolic feat of 358

308 tance [75]. Interestingly, most other members of the tribe turning ingested plant toxins into warning pigmentation 359

309 Mirini have high speciﬁcity for certain host plants to deter predators (e.g., [14 ,90]). For example, the red- 360

310 (reviewed in [76]) and could provide the comparative shouldered soapberry bug Jadera haematoloma has served 361

311 framework for understanding the more generalist polyph- as a model for phenotypic evolution driven by adaptation 362

312 agy of Lygus species. Moreover, phylogenetic relation- to host plants [91,92]. Future genome sequencing for this 363

313 ships within the Cimicomorpha and even its monophyly species would strengthen its ongoing development as a 364

314 remain controversial (Figure 2). The sequencing of mir- species for functional genetics (e.g., Figure 1b). Compar- 365

315 ids, as well as additional reduviids such as the wheel bug ative genomics analysis on these groups will clarify a suite 366

Arilus cristatus, will substantially expand phylogenomic of related features pertaining to metabolism, chemical 367

316 information beyond the present molecular phylogenies tolerance, and the molecular basis of feeding adaptation. 368

317 based on rRNA and mitochondrial genes (e.g., [61,62

318 ,77–79]). Indeed, phylogenies of concatenated, single- Large bug genomes and third generation 369

319 copy orthologues of protein-coding genes, based on ofﬁ- sequencing approaches 370

320 cial gene sets from genome sequencing, have proven Big genomes are challenging, but our computational 371

321 robust and reliable for resolving deeper relationships capabilities are also growing. This will be important as 372

322 among sequenced hemipterans and did preliminarily comparative insect genomics ventures out from the 373

323 recover a cimicomorphan clade based on currently avail- known conﬁnes of the Holometabola to the wider diver- 374

324 able taxa [14 ]. sity of hemimetabolous orders such as the Hemiptera. 375

Although the cicadas’ large genomes are a notable excep- 376

325 Last, but certainly not least, are the Pentatomomorpha, tion on par with the Orthoptera (e.g., [7]), the Hemiptera 377

326 which have one of the richest experimental traditions are a fair representation of genome size ranges among 378

327 among the Hemiptera. For example, landmark mid-twen- hemimetabolous insects [93]. At the larger end of the 379

328 tieth century work in the ﬁrebug Pyrrhocoris apterus dem- spectrum, a quarter of the 5.3-Gb genome was recently 380

329 onstrated the potential impact of environmental phyto- sequenced for the meadow spittlebug, Philaenus spumar- 381

330 chemicals on a species’ endocrine system, which helped ius (Auchenorrhyncha: Aphrophoridae), a research

331 lead to development of juvenile hormone analogs [80,81]. species for phylogeographic studies of speciation and 382

332 Earlier, the ﬁrst animal sex chromosomes were identiﬁed color polymorphism [94]. Although a substantial amount 383

333 in this species in the 1890s (reviewed in [82]). In modern of sequence data (>1 Gb) was already assembled, there 384

334 research, the ﬁrebug is readily amenable to RNAi [16]; it is still a long way to go with this species. As new genome 385

335 has a wealth of salivary gland and gut microbiome tran- sequencing projects are initiated for better taxonomic 386

336 scriptomic data (Figure 2); and an active research com- sampling, genome sizes much greater than 1 Gb will 387

337 munity has recently called for genomic resources to indeed need to be considered carefully in order to 388

338 further advance work on this emerging model for chro- balance biological representation with tractability for 389

339 nobiology [83 ]. Equally, the milkweed bug Oncopeltus generating useful draft-quality genomes. As a guide, 390

fasciatus has served as a long-standing developmental and the Animal Genome Size Database Release 2.0 from 391

340 physiological research model (reviewed in [84]). Its recent 2005 [95] has overestimated the genome sizes of some 392

341 genome sequencing has led to new insights and testable species. For example the genome of O. fasciatus was 393

342 hypotheses on gene structure evolution and the molec- initially estimated at 4.55 Gb [95], compared to recent 394

343 ular bases for feeding ecology differences across the ﬂow cytometry measurements of 926 Mb [14 ]. How- 395

344 Hemiptera [14 ], and this resource is already being ever, the Heteroptera in particular do have medium to 396

345 utilized by the community (e.g., [85,86]). large genomes. 397

346 Future genome projects should build on this foundation Happily, such species will now beneﬁt from recent inno- 398

347 in addressing topics such as feeding ecology. Invasive vations in sequencing approaches. Using long read data, 399

348 pests such as the polyphagous stink bug Halyomorpha high quality hybrid Illumina-PacBio assemblies have 400

halys (Pentatomidae, Figure 2) and the conifer seed bug already been successfully generated for smaller-genome 401

Leptoglossus occidentalis, one of the diverse leaf-footed hemipterans (e.g., 300–600 Mb genomes, [34,36 ]). Fur- 402

349 bugs (Coreidae), have rapidly expanded their geographi- thermore, optical mapping strategies have already sub- 403

350 cal ranges in recent decades. L. occidentalis has spread stantially improved the assembly of large genomes for 404

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Hemipteran diversity through the genomic lens Panfilio and Angelini 7

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contributions to plant decomposition in a fungus-farming

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vertebrates and plants [96–98]. Such approaches would 454

termite. Proc Natl Acad Sci U S A 2014, 111:14500-14505.

406 also support future sequencing projects for large insect

455

10. Harrison MC, Jongepier E, Robertson HM, Arning N, Bitard-Feildel

407 genomes. Given the painstaking cytogenetic work that 456

T, Chao H, Childers CP, Dinh H, Doddapaneni H, Dugan S, et al:

457

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underpins ongoing hemipteran research, such as karyo- Hemimetabolous genomes reveal molecular basis of termite Q4

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eusociality. Nat Ecol Evol. in press.

409 typing that has already been done in P. spumarius and

410 congenerics [99,100], the Hemiptera are well positioned 11. Ioannidis P, Simao FA, Waterhouse RM, Manni M, Seppey M,

Robertson HM, Misof B, Niehuis O, Zdobnov EM: Genomic

411

to continue to thrive in and contribute to the modern 459

features of the damselﬂy Calopteryx splendens representing a

460

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comparative genomics era. sister clade to most insect orders. Genome Biol Evol 2017, 9:415-430. 461

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Comparative genomics analysis beneﬁts from a combination of breadth

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413 Funding and depth in taxon sampling. Early-branching lineages, such as the

464

Odonata, will be particularly important as outgroups for the study of

414 KAP acknowledges project grant A12 of the SFB 680, 465

neopteran insects and their genomes.

415 ‘The Molecular Basis of Evolutionary Innovations’ from

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12. Schuh RT, Slater JA: True Bugs of the World (Hemiptera:

416 the German Research Foundation (DFG) for ﬁnancial 467

Heteroptera), Classiﬁcation and Natural History. Comstock Pub.

417 support during the preparation of this manuscript. Por- Associates; 1995.

418 tions of this material are based upon work supported by 468

Q2 13. Hughes CL, Kaufman TC: RNAi analysis of Deformed,

469

419 National Science Foundation grant IOS-1350207 to DRA. proboscipedia and Sex combs reduced in the

470

milkweed bug Oncopeltus fasciatus: novel roles for

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Hox genes in the Hemipteran head. Development 2000, 127:3683-3694. 472 420 Acknowledgments

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We thank Stephen Richards (Baylor College of Medicine) on behalf of the 14. Panﬁlio KA, Vargas Jentzsch IM, Benoit JB, Erezyilmaz D,

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i5K community for championing insect genomics through the i5K pilot Suzuki Y, Colella S, Robertson HM, Poelchau MF,

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sequencing project and for suggesting the topic of this review. We also Waterhouse RM, Ioannidis P et al.: Molecular evolutionary

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