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Brood is critically important in social insect colonies. It carries the colony’s fitness through delivering future reproductive adults as well as workers that will increase the colony’s workforce. Adoption of non-nestmate brood can increase the colony workforce but entails the risk of rearing unrelated sexuals or social parasites. Thus, theory would predict that ant workers will evolve the ability to discriminate between nestmate and alien brood using the chemical cues displayed at the brood’s surface. This appears especially true for eggs and first instar (L1) larvae, which require more resources before becoming adult workers compared to older brood. However, the chemical signature of ant early brood stages and its recognition by workers remains understudied. To fill this gap, we investigated the chemical basis of early brood nestmate and cross-species recognition in six ant species. We also tested the discrimination behaviour of workers in brood retrieval trials. We observed species-level cues and discrimination against hetero-specific brood. We also found that eggs and most L1 larvae displayed a colony signature. However, only some species discriminated against non-nestmate early brood. Interestingly, these species belong to genera subject to brood parasitism. We hypothesize that non-nestmate brood discrimination could arise from species adaptations against brood parasitism.

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Insect wing polyphenism has evolved as an adaptation to changing environments and a growing body of research suggests that the nutrient-sensing insulin receptor signalling pathway is a hot spot for the evolution of polyphenisms, as it provides a direct link between growth and available nutrients in the environment. However, little is known about the potential role of insulin receptor signalling in polyphenisms which are controlled by seasonal variation in photoperiod. Here, we demonstrate that wing length polyphenism in the water strider Gerris buenoi is determined by photoperiod and nymphal density, but is not directly affected by nutrient availability. Exposure to a long-day photoperiod is highly inducive of the short-winged morph whereas high nymphal densities moderately promote the development of long wings. Using RNA interference we demonstrate that, unlike in several other species where wing polyphenism is controlled by nutrition, there is no detectable role of insulin receptor signalling in wing morph induction. Our results indicate that the multitude of possible cues that trigger wing polyphenism can be mediated through different genetic pathways and that there are multiple genetic origins to wing polyphenism in insects.

International audience; Access to hitherto unexploited ecological opportunities is associated with phenotypic evolution and often results in significant lineage diversification. Yet our understanding of the mechanisms underlying such adaptive traits remains limited. Water striders have been able to exploit the water-air interface, primarily facilitated by changes in the density of hydrophobic bristles and a significant increase in leg length. These two traits are functionally correlated and are both necessary for generating efficient locomotion on the water surface. Whether bristle density and leg length have any cellular or developmental genetic mechanisms in common is unknown. Here, we combine comparative genomics and transcriptomics with functional RNA interference assays to examine the developmental genetic and cellular mechanisms underlying the patterning of the bristles and the legs in Gerris buenoi and Mesovelia mulsanti, two species of water striders. We found that two duplication events in the genes beadex and taxi led to a functional expansion of the paralogs, which affected bristle density and leg length. We also identified genes for which no function in bristle development has been previously described in other insects. Interestingly, most of these genes play a dual role in regulating bristle development and leg length. In addition, these genes play a role in regulating cell division. This result suggests that cell division may be a common mechanism through which these genes can simultaneously regulate leg length and bristle density. We propose that pleiotropy, through which gene function affects the development of multiple traits, may play a prominent role in facilitating access to unexploited ecological opportunities and species diversification.

International audience; Most studies in the field of ecology and evolution aiming to connect genotype to phenotype rarely validate identified loci using functional tools. Recent developments in RNA interference (RNAi) and clustered regularly interspaced palindromic repeats (CRISPR)-Cas genome editing have dramatically increased the feasibility of functional validation. However, these methods come with specific challenges when applied to emerging model organisms, including limited spatial control of gene silencing, low knock-in efficiencies, and low throughput of functional validation. Moreover, many functional studies to date do not recapitulate ecologically relevant variation, and this limits their scope for deeper insights into evolutionary processes. We therefore argue that increased use of gene editing by allelic replacement through homology-directed repair (HDR) would greatly benefit the field of ecology and evolution.

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, they have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. The monophyletic group of water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a group of insects that transited to live on the water-air interface and diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones, representing distinct niches of water surfaces, and further diversification of the group. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

International audience; Gerromorpha, also known as semi-aquatic bugs, present the 7 striking capability to walk on water surface, which has long 8 attracted the interest of many scientists. Yet our understanding 9 of the mechanisms associated with their adaptation and 10 diversification within this new habitat remain largely unknown. 11 In this review we discuss how new transcriptomic and genomic 12 resources have contributed to establish the Gerromorpha as an 13 important lineage to study phenotypic evolution. In particular 14 we outline the impact of recent comparative transcriptomic 15 analyses and first published genomes to advance our 16 understanding of genomic basis of adaptations to water 17 surface locomotion Q3 and sexual dimorphism.

Background Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons. Results We generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Conclusion Our findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

The fauna of semiaquatic bugs (Insecta: Hemiptera: Heteroptera: Gerromorpha) from Panama has been explored mainly between the end of the 19th century and the first half of the 20th century, with few reports since then, whereas that from Colombia has been intensively studied in the last decade. Here, we describe Rhagovelia joceliae Rodrigues & Moreira, sp. nov. (Veliidae: Rhagoveliinae), from Panama. Additionally, new records from these countries are presented for Mesovelia mulsanti White, 1879, Mes. zeteki Harris & Drake, 1941 (Mesoveliidae: Mesoveliinae), Lipogomphus leucostictus (Champion, 1898) (Hebridae: Hebrinae), Hydrometra caraiba Guérin-Méneville, 1857 (Hydrometridae: Hydrometrinae), Platyvelia brachialis (Stål, 1860), Stridulivelia (Stridulivelia) raspa (Hungerford, 1929) (Veliidae: Veliinae), R. elegans Uhler, 1894, R. perija Polhemus, 1997, R. rosensis Padilla-Gil, 2011 (Veliidae: Rhagoveliinae), Euvelia advena Drake, 1957, Microvelia albonotata Champion, 1898, Mi. fantastika Padilla-Gil, 2019, Mi. mimula White, 1879 (Veliidae: Microveliinae), Metrobates laudatus Drake & Harris, 1937, Telmatometra ujhelyii Esaki, 1926 (Gerridae: Trepobatinae), Brachymetra albinervus (Amyot & Serville, 1843) (Gerridae: Charmatometrinae), Potamobates anchicaya Polhemus & Polhemus, 1995 (Gerridae: Cylindrostethinae), Limnogonus hyalinus (Fabricius, 1803), and Tachygerris opacus (Champion, 1898) (Gerridae: Gerrinae).

Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body among individuals of the same population. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented. Here we conduct comparative transcriptomics of the legs followed by an RNA interference (RNAi) screen to identify genes that play a role in the hyperallometric growth of the third legs in the males of the water strider Microvelia longipes. We demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric slope and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope either in the females of M. longipes or in the males and females of other closely related Microvelia species. Furthermore, our data show that a tissue-specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Therefore, male body size, the exaggerated weapon, and the intense fighting behavior associated with it are genetically correlated in M. longipes. Our results support a possible role of pleiotropy in the evolution of allometric slope., Males of the water strider Microvelia longipes possess extremely long legs used as weapons to dominate egg-laying sites; this study shows that the growth factor BMP11 is responsible for increasing body size, leg length and fighting behaviour in these males.

This plot shows that the number of TE superfamilies is correlated to the genome assembly size. (PDF 7 kB)

Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of sex-specific phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the lack of a representative genome and transcriptomes to study the development of secondary sexual traits. Here we present the genome and developmental transcriptomes, focused on the legs of the water striderMicrovelia longipes, a species where males exhibit strikingly long third legs used as weapons. The quality of the genome assembly is such that over 90% of the sequence is captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in sex-biased genes, indicating a specific signature of gene expression in association with sex-specific trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. Interestingly, we found that female-biased genes that are expressed in the third legs only, but not male-biased genes, were over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed that they can arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Our findings shed light on how directional sexual selection drives sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body 1–3. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented 4,5. Here we show that the hyperallometric legs in the males of the water strider Microvelia longipes are associated with a specific signature of gene expression during development. Using RNAi knockdown, we demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric coefficient and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope in females. Furthermore, our data show that a tissue specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Overall, we demonstrate a genetic correlation between male body size, the exaggerated weapon, and the intense fighting behaviour associated with it in M. longipes. Our results provide evidence for a role of pleiotropy in the evolution of allometric slope.

Review history.

Supplementary Text and Supplementary Figures: Figures S1 – S34.

An amendment to this paper has been published and can be accessed via the original article.

Summary Acquisition of new ecological opportunities is a major driver of adaptation and species diversification [1, 2, 3, 4]. However, how groups of organisms expand their habitat range is often unclear [3]. We study the Gerromorpha, a monophyletic group of heteropteran insects that occupy a large variety of water surface-associated niches, from small puddles to open oceans [5, 6]. Due to constraints related to fluid dynamics [7, 8, 9] and exposure to predation [5, 10], we hypothesize that selection will favor high speed of locomotion in the Gerromorpha that occupy water-air interface niches relative to the ancestral terrestrial life style. Through biomechanical assays and phylogenetic reconstruction, we show that only species that occupy water surface niches can generate high maximum speeds. Basally branching lineages with ancestral mode of locomotion, consisting of tripod gait, achieved increased speed on the water through increasing midleg length, stroke amplitude, and stroke frequency. Derived lineages evolved rowing as a novel mode of locomotion through simultaneous sculling motion almost exclusively of the midlegs. We demonstrate that this change in locomotory behavior significantly reduced the requirement for high stroke frequency and energy expenditure. Furthermore, we show how the evolution of rowing, by reducing stroke frequency, may have eliminated the constraint on body size, which may explain the evolution of larger Gerromorpha. This correlation between the diversity in locomotion behaviors and niche specialization suggests that changes in morphology and behavior may facilitate the invasion and diversification in novel environments., Highlights • Semi-aquatic bugs are adapted to life on water surface niches worldwide • Life on the water surface requires high locomotory maximum speed • Increased speed was achieved through changes in leg length and locomotion behavior • Derived lineages evolved rowing, an energy-efficient mode of locomotion on water, During evolution, the semi-aquatic bugs colonized a variety of water surface niches from small puddles to open oceans. Crumière et al. show that access to this new habitat is associated with morphological and behavioral changes that determine locomotory speed. Variation in locomotion behavior in distinct lineages is correlated with niche specialization.

Significance Understanding how existing genomic content can be reused to generate new phenotypes is important for understanding how species diversify. Here, we address this question by studying the origin of a phenotype consisting of bright coloration in the embryos of water striders. We found that the pteridine biosynthesis pathway, originally active in the eyes, has been coopted in the embryo to produce various colors in the antennae and legs. The coopted pathway remained stable for over 200 million years, yet resulted in a striking diversification of colors and color patterns during the evolution of water striders. This work demonstrates how the activation of a complete pathway in new developmental contexts can drive the evolution of novelty and fuel species diversification., Naturalists have been fascinated for centuries by animal colors and color patterns. While widely studied at the adult stage, we know little about color patterns in the embryo. Here, we study a trait consisting of coloration that is specific to the embryo and absent from postembryonic stages in water striders (Gerromorpha). By combining developmental genetics with chemical and phylogenetic analyses across a broad sample of species, we uncovered the mechanisms underlying the emergence and diversification of embryonic colors in this group of insects. We show that the pteridine biosynthesis pathway, which ancestrally produces red pigment in the eyes, has been recruited during embryogenesis in various extraocular tissues including antennae and legs. In addition, we discovered that this cooption is common to all water striders and initially resulted in the production of yellow extraocular color. Subsequently, 6 lineages evolved bright red color and 2 lineages lost the color independently. Despite the high diversity in colors and color patterns, we show that the underlying biosynthesis pathway remained stable throughout the 200 million years of Gerromorpha evolutionary time. Finally, we identified erythropterin and xanthopterin as the pigments responsible for these colors in the embryo of various species. These findings demonstrate how traits can emerge through the activation of a biosynthesis pathway in new developmental contexts.

Sexually selected traits can reach high degrees of phenotypic expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait evolution is poorly understood. In the water strider Microvelia longipes , males display striking trait exaggeration and phenotypic variation manifested as extreme differences in the rear leg length. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioural, morphometric and reaction norm experiments in a selection of Microvelia species. We uncovered differences both in the mating behaviour and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behaviour where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Through male–male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

Background: The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae. Results: The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted the evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid nutrition feeding. Conclusions: With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus’s strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes., La lista completa de autores puede verse en el archivo asociado., Facultad de Ciencias Exactas, Centro Regional de Estudios Genómicos

Small open reading frames (smORFs) encoding ‘micropeptides’ exhibit remarkable evolutionary complexity. Conserved peptides encoded by mille-pattes (mlpt)/polished rice (pri)/tarsal less (tal) are essential for embryo segmentation in Tribolium but, in Drosophila, function in terminal epidermal differentiation and patterning of adult legs. Here, we show that a molecular complex identified in Drosophila epidermal differentiation, comprising Mlpt peptides, ubiquitin-ligase Ubr3 and transcription factor Shavenbaby (Svb), represents an ancient developmental module required for early insect embryo patterning. We find that loss of segmentation function for this module in flies evolved concomitantly with restriction of Svb expression in early Drosophila embryos. Consistent with this observation, artificially restoring early Svb expression in flies causes segmentation defects that depend on mlpt function, demonstrating enduring potency of an ancestral developmental switch despite evolving embryonic patterning modes. These results highlight the evolutionary plasticity of conserved molecular complexes under the constraints of essential genetic networks.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

Sexually selected traits can reach high degrees of phenotypic expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait evolution is poorly understood. In the water strider Microvelia longipes, males display striking trait exaggeration and phenotypic variation manifested as extreme differences in the rear leg length. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioural, morphometric and reaction norm experiments in a selection of Microvelia species. We uncovered differences both in the mating behaviour and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behaviour where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Through male–male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

Alu alignments. These plots illustrate that copies of the SINE Alu are present in 56 of the genomes under study. Grey sections in the alignments are positions identical to the canonical Alu sequence at the top. (PDF 4480 kb)

Supplementary notes, figures, and small tables. (PDF 6142 kb)

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 strider genome hinders our ability to more thoroughly investigate the molecular mechanisms underlying the processes of adaptation and diversification within this group. Results Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome; the first water strider genome to be sequenced thus far. The size of the G. buenoi genome is approximately 1,000 Mb, and this sequencing effort has recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to a water surface lifestyle. These expansions may affect key processes associated with growth, vision, desiccation resistance, detoxification, olfaction and epigenetic regulation. Strikingly, the G. buenoi genome contains three insulin receptors, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes affecting with opsin genes may be associated with wavelength sensitivity shifts in opsins, which is likely to be key in facilitating specific adaptations in vision for diverse water habitats. Conclusions Our findings suggest that local gene duplications might have played an important role during the evolution of water striders. Along with these findings, the sequencing of the G. buenoi genome now provides us the opportunity to pursue exciting research opportunities to further understand the genomic underpinnings of traits associated with the extreme body plan and life history of water striders. Electronic supplementary material The online version of this article (10.1186/s12864-018-5163-2) contains supplementary material, which is available to authorized users.

The semi-aquatic bugs (Heteroptera, Gerromorpha) conquered water surfaces worldwide and diversified to occupy puddles, ponds, streams, lakes, mangroves and even oceans. Critical to this lifestyle is the evolution of sets of hairs that allow these insects to maintain their body weight on the water surface and protect the animals against wetting and drowning. In addition, the legs of these insects are equipped with various grooming combs that are important for cleaning and tidying the hair layers for optimal functional efficiency. Here we show that the hairs covering the legs of water striders represent innervated bristles. Genomic and transcriptomic analyses revealed that in water striders the achaete–scute complex, known to control bristle development in flies, contains only the achaete–scute homologue (ASH) gene owing to the loss of the gene asense. Using RNA interference, we show that ASH plays a pivotal role in the development of both bristles and grooming combs in water striders. Our data suggest that the ASH locus may have contributed to the adaptation to water surface lifestyle through shaping the hydrophobic bristles that prevent water striders from wetting and allow them to exploit water surface tension.

SummarySmall open reading frames (smORFs) that code for “micropeptides” (10-100 amino acids) exhibit remarkable evolutionary complexity. Conserved micropeptides encoded by themillepattes (mlpt)gene are essential inTriboliumfor embryogenesis but inDrosophila,function only in leg and cuticle differentiation. We find that a module identified inDrosophilatrichome patterning, comprising Mlpt, UBR3, and Shaven-baby (Svb), coordinates early embryo patterning in several insect orders. Intriguingly, Mlpt segmentation function can be re-awakened in theDrosophilablastoderm, demonstrating the potency of an ancestral developmental switch retained despite evolving embryonic patterning modes. smORFs likemillepattesthus illustrate plasticity of micropeptide functions despite constraints of essential genetic networks.One sentence summaryA module comprising the small ORFs mlpt/pri/tal, the transcription factor Svb, and the ubiquitin ligase UBR3, possesses an ancestral function in insect embryo patterning which is lost in flies but reactivated when Svb expression is restored.

Rhagovelia apuruaque sp. nov. (Hemiptera: Heteroptera: Veliidae), from the commune of Régina, French Guiana, is described, illustrated, and compared with species of the salina group. Brachymetra albinervus (Amyot & Serville, 1843), B. lata Shaw, 1933, Limnogonus ignotus Drake & Harris, 1934, Neogerris lubricus (White, 1879), Rheumatobates crassifemur esakii Schroeder, 1931 (Gerridae), Mesovelia mulsanti White, 1879 (Mesoveliidae), Microvelia longipes Uhler, 1894, M. mimula White, 1879, M. pulchella Westwood, 1834, R. humboldti Polhemus, 1997, and S. transversa (Hungerford, 1929) (Veliidae) are recorded for the first time from French Guiana. The presence of Tachygerris adamsoni (Drake, 1942) (Gerridae) in the country is confirmed. New records are presented for the following species previously reported from the study area: B. shawi Hungerford & Matsuda, 1957, Cylindrostethus palmaris Drake & Harris, 1934, L. hyalinus (Fabricius, 1803) (Gerridae), Husseyella turmalis (Drake & Harris, 1933), Paravelia bullialata Polhemus & Polhemus, 1984, and Stridulivelia strigosa (Hungerford, 1929) (Veliidae).

Finet_Figures_Tables_ESM.pdf

Nucleotide sequences of Insulin receptors genes annotated in Gerromorpha (Gerris buenoi, Aquarius paludum, Limnoporus dissortis, Rhagovelia antilleana, Microvelia longipes, Mesovelia furcata, Hydrometra cumata and Hebrus sp). (DOCX 40kb)

Protein sequences of annotated chemoreceptors in Gerris buenoi : 155 Or, 135 Gr and 45 IR genes. (DOCX 83 kb)

Gerris buenoi serosins nucleotide and protein sequences. (DOCX 12 kb)

Fans enable water strider adaptation Genomes of closely related organisms are similar but contain variations that enable different phenotypes and lifestyles. The origin of evolutionary innovations, such as insect wings and bird feathers, poses a challenge to evolutionary biology because the de novo emergence of complex traits cannot easily be explained by natural selection. Water-walking Rhagovelia insects evolved a propelling fan on the middle leg that is associated with life on fast-flowing streams. Santos et al. discovered that the geisha and mother-of-geisha genes underlie fan development and evolution and that this evolutionary innovation is essential to the adaptation of Rhagovelia to its environment. Thus, the evolution of taxon-restricted genes can contribute directly to taxon-restricted novelties that allow access to unexploited ecological niches. Science , this issue p. 386

Growth control scales morphological attributes and, therefore, provides a critical contribution to the evolution of adaptive traits. Yet, the genetic mechanisms underlying growth in the context of specific ecological adaptations are poorly understood. In water striders, adaptation to locomotion on the water surface is associated with allometric and functional changes in thoracic appendages, such that T2-legs, used as propelling oars, are longer than T3-legs, used as steering rudders. The Hox gene Ubx establishes this derived morphology by elongating T2-legs but shortening T3-legs. Using gene expression assays, RNAi knockdown, and comparative transcriptomics, we demonstrate that the evolution of water surface rowing as a novel means of locomotion is associated with the evolution of a dose-dependent promoting-repressing effect of Ubx on leg growth. In the water strider Limnoporus dissortis, T3-legs express six to seven times higher levels of Ubx compared to T2-legs. Ubx RNAi shortens T2-legs and the severity of this phenotype increases with increased depletion of Ubx protein. Conversely, Ubx RNAi lengthens T3-legs but this phenotype is partially rescued when Ubx protein is further depleted. This dose-dependent effect of Ubx on leg growth is absent in non-rowing relatives that retain the ancestral relative leg length. We also show that the spatial patterns of expression of dpp, wg, hh, egfr, dll, exd, hth, and dac are unchanged in Ubx RNAi treatments. This indicates that the dose-dependent opposite effect of Ubx on T2- and T3-legs operates without any apparent effect on the spatial expression of major leg patterning genes. Our data suggest that scaling of adaptive allometries can evolve through changes in the levels of expression of Hox proteins early during ontogeny, and in the sensitivity of the tissues that express them, without any major effects on pattern formation., Highlights • Ubx is generally expressed at higher levels in T3- relative to T2-legs in semi-aquatic insects. • It is only in the derived Gerridae where the high levels of Ubx result in reduced T3-leg length. • In the Gerridae, the response of leg tissues to Ubx levels is bimodal. • Changes in Ubx regulation and function have evolved in Limnoporus without disrupting patterning hierarchies. • Changes in Hox protein levels and emergence of tissue sensitivity to these levels can shape adaptive morphological traits.

Ants are some of the most abundant and familiar animals on Earth, and they play vital roles in most terrestrial ecosystems. Although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. Here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive Argentine ant ( Linepithema humile ), which was accomplished using a combination of 454 (Roche) and Illumina sequencing and community-based funding rather than federal grant support. Manual annotation of >1,000 genes from a variety of different gene families and functional classes reveals unique features of the Argentine ant's biology, as well as similarities to Apis mellifera and Nasonia vitripennis . Distinctive features of the Argentine ant genome include remarkable expansions of gustatory (116 genes) and odorant receptors (367 genes), an abundance of cytochrome P450 genes (>110), lineage-specific expansions of yellow/major royal jelly proteins and desaturases, and complete CpG DNA methylation and RNAi toolkits. The Argentine ant genome contains fewer immune genes than Drosophila and Tribolium , which may reflect the prominent role played by behavioral and chemical suppression of pathogens. Analysis of the ratio of observed to expected CpG nucleotides for genes in the reproductive development and apoptosis pathways suggests higher levels of methylation than in the genome overall. The resources provided by this genome sequence will offer an abundance of tools for researchers seeking to illuminate the fascinating biology of this emerging model organism.

Trait exaggeration, well known to naturalists and evolutionary biologists, has recently become a prominent research subject in the modern field of Evolutionary Developmental Biology. A large number of traits that can be considered as cases of exaggeration exist in nature. Yet, the field has almost exclusively focused on the study of growth-related exaggerated traits in a selection of holometabolous insects. The absence of the hemimetabola from studies of exaggeration leaves a significant gap in our understanding of the development and evolution of such traits. Here we argue that efforts to understand the mechanisms of trait exaggeration would benefit from expanding the study subjects to include other kinds of exaggeration and other model species.