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Aspects of the biology of water striders. a Adult Gerris sp on water and zoom in on the bristles allowing this adaptation using Scanning Electron Microscopy (insets). bG. buenoi rowing on the water surface, illustrating the adaptive locomotion mode. c Water strider jumping using its long legs to escape the strike of a surface hunting fish. d Hoarding behavior in water striders consisting of multiples individuals feeding on a cricket trapped by surface tension. e Wing polymorphism in G. buenoi, here illustrated by three distinct morphs with regard to wing size
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Background
Having conquered water surfaces worldwide, the semi-aquatic bugs occupy ponds, streams, lakes, mangroves, and even open oceans. The diversity of this group has inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water stri...
Citations
... Food contamination is not new, but it is worth noting that many researchers still ignore the contamination from the digestive system when sequencing the target species of our study. For instance, in Hemiptera, we detected contamination from Orthoptera, likely because live crickets were used to feed the water striders, as recorded in the methods and materials [33]. This is not an isolated case, as feeding pea aphids to Hippodamia convergens (Coleoptera, Coccinellidae) [34] and rearing soybean aphids (Hemiptera, Aphididae) to Aphelinus certus (Hymenoptera, Aphelinidae) have also been documented [35]. ...
The rapid advancement of high-throughput sequencing has led to a great increase in sequencing data, resulting in a significant accumulation of contamination, for example, sequences from non-target species may be present in the target species’ sequencing data. Insecta, the most diverse group within Arthropoda, still lacks a comprehensive evaluation of contamination prevalence in public databases and an analysis of potential contamination causes. In this study, COI barcodes were used to investigate contamination from insects and mammals in GenBank’s genomic and transcriptomic data across four insect orders. Among the 2796 WGS and 1382 TSA assemblies analyzed, contamination was detected in 32 (1.14%) WGS and 152 (11.0%) TSA assemblies. Key findings from this study include the following: (1) TSA data exhibited more severe contamination than WGS data; (2) contamination levels varied significantly among the four orders, with Hemiptera showing 9.22%, Coleoptera 3.48%, Hymenoptera 7.66%, and Diptera 1.89% contamination rates; (3) possible causes of contamination, such as food, parasitism, sample collection, and cross-contamination, were analyzed. Overall, this study proposes a workflow for checking the existence of contamination in WGS and TSA data and some suggestions to mitigate it.
... The libraries were sequenced either on Illumina HiSeq X or NovaSeq 6000 (150 bp paired-end). We targeted a minimum of 3 Gbp of sequence reads per sample, based on 2-3 × sequencing coverage recommended by Tan et al. (2021) for genome skimming, and the known ~1 Gbp Gerris buenoi Kirkaldy, 1911 genome size (Armisén et al. 2018). ...
Gerromorpha Popov, 1971 is a fascinating and diverse insect lineage that evolved about 200 Mya to spend their entire life cycle on the air-water interface and have since colonized all types of aquatic habitats. The sub-family Halobatinae Bianchi, 1896 is particularly interesting because some species have adapted to life on the open ocean-a habitat where insects are very rarely found. Several attempts have been made to reconstruct the phylogenetic hypotheses of this subfamily, but the use of a few partial gene sequences recovered only a handful of well-supported relationships, thus limiting evolutionary inferences. Fortunately, the emergence of high-throughput sequencing technologies has enabled the recovery of more genetic markers for phylogen-etic inference. We applied genome skimming to obtain mitochondrial and nuclear genes from low-coverage whole-genome sequencing of 85 specimens for reconstructing a well-supported phylogeny, with particular emphasis on Halobatinae. Our study confirmed that Metrocorini Matsuda, 1960, is paraphyletic, whereas Esakia Lundblad, 1933, and Ventidius Distant, 1910, are more closely related to Halobatini Bianchi, 1896, than Metrocoris Mayr, 1865, and Eurymetra Esaki, 1926. We also found that Ventidius is paraphyletic and in need of a taxonomic revision. Ancestral state reconstruction suggests that Halobatinae evolved progressively from limnic to coastal habitats, eventually attaining a marine lifestyle, especially in the genus Halobates Eschscholtz, 1822, where the oceanic lifestyle evolved thrice. Our results demonstrate that genome skimming is a powerful and straightforward approach to recover genetic loci for robust phylogenetic analysis in non-model insects.
... Studies investigating dietary variations in Hemiptera revealed that within this insect order, Acyrthosiphon pisum, whitefly, Laodelphax striatellus, Oncopeltus fasciatus, and Riptortus pedestris are classified as phytophagous insects (Li et al., 2017). On the other hand, T. rubrofasciata, R. prolixus, C. lectularius, and Gerris buenoi are carnivorous insects (Rosenfeld et al., 2016;Armisén et al., 2018;Liu et al., 2019;Huang et al., 2021;Rijal et al., 2021). Except G. buenoi, the habitats of these insects are primarily semi-aquatic (Armisén et al., 2018). ...
... On the other hand, T. rubrofasciata, R. prolixus, C. lectularius, and Gerris buenoi are carnivorous insects (Rosenfeld et al., 2016;Armisén et al., 2018;Liu et al., 2019;Huang et al., 2021;Rijal et al., 2021). Except G. buenoi, the habitats of these insects are primarily semi-aquatic (Armisén et al., 2018). ...
... prolixus from the Cimicomorpha suborder, and G. buenoi from the Gerromorpha suborder (Armisén et al., 2018;Liu et al., 2019;Huang et al., 2021). There is also a haematophagous species, C. lectularius, which belongs to the Cimicomorpha suborder. ...
Hemiptera insects exhibit a close relationship to plants and demonstrate a diverse range of dietary preferences, encompassing phytophagy as the predominant feeding habit while a minority engages in carnivorous or haematophagous behaviour. To counteract the challenges posed by phytophagous insects, plants have developed an array of toxic compounds, causing significant evolutionary selection pressure on these insects. In this study, we employed a comparative genomics approach to analyse the expansion and contraction of gene families specific to phytophagous insect lineages, along with their adaptive evolutionary traits, utilising representative species from the Hemiptera order. Our investigation revealed substantial expansions of gene families within the phytophagous lineages, especially in the Pentatomomorpha branch represented by Oncopeltus fasciatus and Riptortus pedestris. Notably, these expansions of gene families encoding enzymes are potentially involved in hemipteran-plant interactions. Moreover, the adaptive evolutionary analysis of these lineages revealed a higher prevalence of adaptively evolved genes in the Pentatomomorpha branch. The observed branch-specific gene expansions and adaptive evolution likely contribute significantly to the diversification of species within Hemiptera. These results help enhance our understanding of the genomic characteristics of the evolution of different feeding habits in hemipteran insects.
... The spectral sensitivities of an organism are directly linked to its opsin gene content and expression; thus, this gene family provides a useful framework to relate changes in the genotype to the evolution of visual adaptations and behaviors (Arikawa 2017;Hauser and Chang 2017;van der Kooi et al. 2021;Van Nynatten et al. 2021). Opsin gene duplication and divergence, and gene loss, are 2 mechanisms by which insects have evolved altered visual sensitivities to adapt to niche-specific light environments and external cues (Spaethe and Briscoe 2004;Frentiu et al. 2007;Briscoe 2008;Thoen et al. 2014;Futahashi et al. 2015;Chen et al. 2016;Feuda et al. 2016;Sharkey et al. 2017;Armisén et al. 2018;Almudi et al. 2020;Feuda et al. 2021;Sondhi et al. 2021;Guignard et al. 2022;McCulloch, Macias-Muñoz, Mortazavi, et al. 2022). However, other mechanisms are known to increase the diversity of opsin specificities resulting in variation in light-sensing abilities, such as amino acid substitutions without gene duplication causing shifts in absorption spectra (Shichida and Matsuyama 2009;Wakakuwa et al. 2010;Hauser et al. 2014;Liénard et al. 2021;Sharkey et al. 2023), coexpression of certain opsin proteins in a single photoreceptor cell (Wakakuwa et al. 2004;Perry et al. 2016;Satoh et al. 2017;Macias-Muñoz et al. 2019;Ilić et al. 2022), differences in ommatidia structure of the compound eye (Lau and Gross 2007;Lau and Meyer-Rochow 2007), and paralog-specific opsin gene expression (Arikawa 2003;Perry et al. 2016;Finkbeiner and Briscoe 2021;Roberts et al. 2023). ...
Color vision in insects is determined by signaling cascades, central to which are opsin proteins, resulting in sensitivity to light at different wavelengths. In certain insect groups, lineage-specific evolution of opsin genes, in terms of copy number, shifts in expression patterns, and functional amino acid substitutions, has resulted in changes in color vision with subsequent behavioral and niche adaptations. Lepidoptera are a fascinating model to address whether evolutionary change in opsin content and sequence evolution are associated with changes in vision phenotype. Until recently, the lack of high-quality genome data representing broad sampling across the lepidopteran phylogeny has greatly limited our ability to accurately address this question. Here, we annotate opsin genes in 219 lepidopteran genomes representing 33 families, reconstruct their evolutionary history, and analyze shifts in selective pressures and expression between genes and species. We discover 44 duplication events in opsin genes across ∼300 million years of lepidopteran evolution. While many duplication events are species or family specific, we find retention of an ancient long-wavelength-sensitive (LW) opsin duplication derived by retrotransposition within the speciose superfamily Noctuoidea (in the families Nolidae, Erebidae, and Noctuidae). This conserved LW retrogene shows life stage-specific expression suggesting visual sensitivities or other sensory functions specific to the early larval stage. This study provides a comprehensive order-wide view of opsin evolution across Lepidoptera, showcasing high rates of opsin duplications and changes in expression patterns.
... First insights into the genomic dimensions of hemipteran diversification have been gained through the genome sequence assemblies for a number of key species [4], starting with the pea aphid Acyrtosiphon pisum [11], the kissing bug Rhodnius prolixus [3], and the bed bug Cimex lectularius [1]. Subsequent efforts added genomes from specialist species, like the water strider Gerris buenoi [12], the laboratory model Oncopeltus fasciatus [13], and the closely related pentatomid stink bug Halyomorpha halys [14]. Today, over 80 hemipteran genome assemblies are available through the National Center for Biotechnology Information (NCBI) [15] for deeper studies of gene families of interest. ...
... Less expected, however, was the genomic evidence of the lack of B-opsins in the pea aphid, A. pisum [11,22]. Equally surprising, the genome-wide analyses of the opsin repertoires of the water strider, G. buenoi, and the milkweed bug, O. fasciatus, also failed to detect B-opsins [12,13]. Consistent with a general absence of B-opsins in the Heteroptera [23] reported the conservation of LW-and UV-opsins but an absence of B-opsin in plant bugs (Heteroptera: Miridae). ...
... While the lack of B-opsins from hemipteran taxa as distantly related as aphids and Heteroptera raised the possibility of an early loss of this subfamily during hemipteran diversification, the documentation of B-opsin in the green rice leafhopper Nephotettix cincticeps (Auchenorrhyncha: Cicadomorpha) pointed to a more complex scenario [24]. Moreover, transcriptome searches recovered a B-opsin homolog in the hackberry petiole gall psyllid Pachypsylla venusta (Sternorrhyncha) [12]. Corroborating the conservation of Bopsin in the Sternorrhyncha, a B-opsin homolog was recently also reported from the Asian citrus psyllid Diaphorina citri [25]. ...
Simple Summary
Hemiptera is one of the largest and most diverse insect orders, yet our knowledge about visual opsin evolution in this group remains preliminary. This study provides an updated survey of visual opsin genes in the Hemiptera, which reveals that the subfamily of blue-sensitive opsin receptor genes has been independently lost in planthoppers and aphids. Moreover, in both groups, tandem duplication of UV-sensitive opsins produced sister paralogs that diverged by maintaining ancestral UV sensitivity versus shifting to blue sensitivity and thereby likely compensating for the loss of the blue-sensitive opsin subfamily. The study further shows that these parallel trajectories at the level of gene family evolution are associated with mostly convergent changes at the level of protein sequence evolution.
Abstract
Expanding on previous efforts to survey the visual opsin repertoires of the Hemiptera, this study confirms that homologs of the UV- and LW-opsin subfamilies are conserved in all Hemiptera, while the B-opsin subfamily is missing from the Heteroptera and subgroups of the Sternorrhyncha and Auchenorrhyncha, i.e., aphids (Aphidoidea) and planthoppers (Fulgoroidea), respectively. Unlike in the Heteroptera, which are characterized by multiple independent expansions of the LW-opsin subfamily, the lack of B-opsin correlates with the presence of tandem-duplicated UV-opsins in aphids and planthoppers. Available data on organismal wavelength sensitivities and retinal gene expression patterns lead to the conclusion that, in both groups, one UV-opsin paralog shifted from ancestral UV peak sensitivity to derived blue sensitivity, likely compensating for the lost B-opsin. Two parallel bona fide tuning site substitutions compare to 18 non-corresponding amino acid replacements in the blue-shifted UV-opsin paralogs of aphids and planthoppers. Most notably, while the aphid blue-shifted UV-opsin clade is characterized by a replacement substitution at one of the best-documented UV/blue tuning sites (Rhodopsin site 90), the planthopper blue-shifted UV-opsin paralogs retained the ancestral lysine at this position. Combined, the new findings identify aphid and planthopper UV-opsins as a new valuable data sample for studying adaptive opsin evolution.
... If any extinction event is correlated with these shifts, the end-Cretaceous mass extinction or even smaller events during the Cenozoic such as the Eocene thermal maximum or Eocene-Oligocene transition are seemingly most likely. The genome of H. lingyangjiaoensis is of a medium size for true bugs (0.68-1.55 Gb) [68,69] and a similar size to those of other semi-aquatic bugs [70,71]. Comparative genomic analyses with other arthropod species show that the gene families functioning in the moulting cycle and related processes are significantly contracted, which certainly relates to their reduced life cycles. ...
Among hundreds of insect families, Hermatobatidae (commonly known as coral treaders) is one of the most unique. They are small, wingless predac-eous bugs in the suborder Heteroptera. Adults are almost black in colour, measuring about 5 mm in body length and 3 mm in width. Thirteen species are known from tropical coral reefs or rocky shores, but their origin and evolutionary adaptation to their unusual marine habitat were unexplored. We report here the genome and metagenome of Hermatobates lingyangjiaoensis, hitherto known only from its type locality in the South China Sea. We further reconstructed the evolutionary history and origin of these marine bugs in the broader context of Arthropoda. The dated phylogeny indicates that Hexapoda diverged from their marine sister groups approximately 498 Ma and that Hermatobatidae originated 192 Ma, indicating that they returned to an oceanic life some 300 Myr after their ancestors became terrestrial. Their origin is consistent with the recovery of tropical reef ecosystems after the end-Triassic mass extinction, which might have provided new and open niches for them to occupy and thrive. Our analyses also revealed that both the genome changes and the symbiotic bacteria might have contributed to adaptations necessary for life in the sea.
... Auchenorrhynchan, can walk on water, while the Sternorrhynchan cannot walk and survive on water, which is perhaps related to FARs (Armisen et al., 2018;De Barro et al., 2011;Li et al., 2019;Oke et al., 2020). One of the functions of FARs from N. lugens is to play an important role in the production of CHC, which plays a crucial role in water resistance (Chung & Carroll, 2015). ...
... aquatic Hemipteran species commonly found in freshwater areas such as lakes, ponds, rice fields and wetlands that can walk on water without breaking the surface or getting its legs wet (Armisen et al., 2018). ...
Fatty acyl-CoA reductases (FARs) play an important role in the synthesis of fatty alcohols in various organisms. Based on the important function of FAR genes, they can be used as a potential molecular target for controlling agricultural pests. Although the FAR genes have been studied in a number of insects, the gain, loss, and molecular evolution of FAR genes between different Hemipteran species still require comprehensive and systematic
study. This study systematically identified and analysed 352 FAR genes from 12 Hemipteran species, including six typical true bug species, Cimex lectularius, Apolygus lucorum, Halyomorpha halys, Oncopeltus fasciatus, Rhodnius prolixus and Gerris buenoi. The number of FAR genes per species ranged from 17 to 43, and a phylogenetic analysis showed that the identified FAR genes of Hemiptera can be classified into 11 clades. The gain and loss
of FAR genes have occurred in some Hemipteran species. These FAR genes conform to the birth-and-death model in the evolutionary process. Through selection pressure analysis, we determined that G. buenoi in clade 11 evolved under the pressure of positive selection, with the evolutionary sites of A at position 214 and T at position 451, thus clarifying the differences in amino acids among species and providing a better understanding of the molecular evolutionary mechanism of Hemipteran FAR. In addition, structural analysis of the FAR genes revealed duplication of the two conservative domains, the Rossmann-fold domain and the sterile domain, of the FAR in four species, namely Bemisia tabaci, Diaphorina citri, R. prolixus and Trialeurodes vaporariorum. This study lays a foundation for further studies on the molecular functions of Hemiptera FAR, and provides a possible new target for the control of Hemiptera, especially the stink bugs.
... First insights into the genomic dimensions of hemipteran diversification have been gained through the genome sequence assemblies for a number of key species [4], starting with the pea aphid Acyrtosiphon pisum [9], the kissing bug Rhodnius prolixus [2] and the bed bug Cimex lectularius [1]. Subsequent efforts added genome assemblies from specialist species like the water strider Gerris buenoi [10], the established laboratory model Oncopeltus fasciatus [11], and the closely related pentatomid stink bug Halyomorpha halys [12]. Today, over 80 hempiteran genome assemblies are available through the National Center for Biotechnology Information (NCBI) [13] for deeper studies of gene families of interest. ...
... Less expected, however, was the genomic evidence of the lack of B-opsins in the pea aphid A. pisum [2,3,19]. Equally surprising, also the genome-wide analyses of the opsin repertoires of the water strider, G. buenoi, and the milkweed bug, O. fasciatus, failed to detect B-opsins [10,11]. Conistent with a general absence of B-opsins in the Heteroptera, [20] reported the conservation of LW-and UV-opsins but absence of B-opsin in plant bugs (Heteroptera: Miridae). ...
... While the lack of B-opsins from hemipteran taxa as distantly related as aphids and Heteroptera raised the possibility of an early loss of this subfamily during hemipteran diversification, the documentation of B-opsin in the green rice leafhopper Nephotettix cincticeps (Auchenorrhyncha: Cicadomorpha) pointed to a more complex scenario [21]. Moreover, transcriptome searches recovered a B-opsin homolog in the hackberry petiole gall psyllid Pachypsylla venusta (Sternorrhyncha) [10]. Corroborating the conservation of B-opsin in the Sternorrhyncha, a B-opsin homolog was recently also reported from the Asian citrus psyllid Diaphorina citri [22]. ...
Expanding previous efforts to survey the visual opsin repertoires of the Hemiptera, this study confirms that homologs of the UV- and LW-opsin subfamilies are conserved in all Hemiptera, while the B-opsin subfamily is missing from the Heteroptera and subgroups of the Sternorrhyncha and Auchenorrhyncha, i.e. aphids (Aphidoidea) and planthoppers (Fulgoroidea), respectively. Unlike in the Heteroptera, which are characterized by multiple expansions of the LW-opsin subfamily, the lack of B-opsin correlates with the presence of tandem-duplicated UV-opsins in aphids and planthoppers. Available data on organismal wavelength sensitivities and retinal gene expression patterns lead to the conclusion that, in both groups, one UV-opsin paralog shifted from ancestral UV peak sensitivity to derived blue sensitivity, thereby compensating for the lost B-opsin. Two parallel bona fide tuning site substitutions compare to 18 non-corresponding amino acid replacements in the blue-shifted UV-opsin paralogs of aphids and planthoppers. Most notably, while the aphid blue-shifted UV-opsin clade is characterized by a replacement substitution at one of the best-documented UV/blue tuning sites (Rhodopsin site 90), the planthopper blue-shifted UV-opsin paralogs retained the ancestral lysine at this position. The combined findings identify aphid and planthopper UV-opsins as a new valuable data sample for studying adaptive opsin evolution.
... LW opsin duplications also occurred in the family Gerridae (water striders) (Guignard et al., 2022). LW opsins in the water strider Gerris buenoi are predicted to be short wavelength shifted, accounting for the blue-light sensitivity recorded from this species (Armis en et al., 2018) considering that no SW opsins have been identified in this group (Guignard et al., 2022). Like duplications of the UV opsin class following loss of SW opsins in Coleoptera, LW opsin duplications may counteract loss of other opsin classes. ...
Many animals depend on the sense of vision for survival. In eumetazoans, vision requires specialized, light-sensitive cells called photoreceptors. Light reaches the photoreceptors and triggers the excitation of light-detecting proteins called opsins. Here, we describe the story of visual opsin evolution from the ancestral bilaterian to the extant vertebrate lineages. We explain the mechanisms determining color vision of extant vertebrates, focusing on opsin gene losses, duplications, and the expression regulation of vertebrate opsins. We describe the sequence variation both within and between species that has tweaked the sensitivities of opsin proteins towards different wavelengths of light. We provide an extensive resource of wavelength sensitivities and mutations that have diverged light sensitivity in many vertebrate species and predict how these mutations were accumulated in each lineage based on parsimony. We suggest possible natural and sexual selection mechanisms underlying these spectral differences. Understanding how molecular changes allow for functional adaptation of animals to different environments is a major goal in the field, and therefore identifying mutations affecting vision and their relationship to photic selection pressures is imperative. The goal of this review is to provide a comprehensive overview of our current understanding of opsin evolution in vertebrates.
... In insects, we see LWRh evolution by both of these mechanisms and probably others that are not as easy to identify. In the water strider Gerris buenoi and in Anopheles gambiae, four and five LWRh genes, respectively, are located in tandem [110,122]. Some LWRh paralogues in moths and Anopheles are intronless and are proposed to have evolved by retrotransposition [109,111,124]. ...
... The numbers in the boxes show number of gene copies present in that species. Figure made using data from [7,78,100,101,[109][110][111][112][113][114][115][116]. ...
The visual pigments known as opsins are the primary molecular basis for colour vision in animals. Insects are among the most diverse of animal groups and their visual systems reflect a variety of life histories. The study of insect opsins in the fruit fly Drosophila melanogaster has led to major advances in the fields of neuroscience, development and evolution. In the last 25 years, research in D. melanogaster has improved our understanding of opsin genotype–phenotype relationships while comparative work in other insects has expanded our understanding of the evolution of insect eyes via gene duplication, coexpression and homologue switching. Even so, until recently, technology and sampling have limited our understanding of the fundamental mechanisms that evolution uses to shape the diversity of insect eyes. With the advent of genome editing and in vitro expression assays, the study of insect opsins is poised to reveal new frontiers in evolutionary biology, visual neuroscience, and animal behaviour.
This article is part of the theme issue ‘Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods’.
