The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

Abstract

BackgroundHaving 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.ResultsHere 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.ConclusionsOur 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 materialThe online version of this article (10.1186/s12864-018-5163-2) contains supplementary material, which is available to authorized users.

Evolution of the Torso activation cassette, a pathway required for terminal patterning and moulting

“…Torso-like has been duplicated several times within lineages of the Pancrustacea including in the Hemiptera, where there are apparent lineage-specific duplications of the gene in the pea aphid (Ac. pisum; Shigenobu et al, 2010;Bickel et al, 2013;Duncan et al, 2013), the kissing bug (R. prolixus; Mesquita et al, 2015) and the water strider (Gerris buenoi; Armisen et al, 2018). In this study, we have also identified a duplication of torso-like within the Lepidoptera, occurring prior to the diversification of moths and butterflies 250 Ma, with two copies of this gene maintained in the genomes of all sequenced lepidopteran species.…”

“…pisum; Shigenobu et al, 2010;Bickel et al, 2013;Duncan et al, 2013), the kissing bug (R. prolixus; Mesquita et al, 2015) and the water strider (Gerris buenoi; Armisen et al, 2018). Although it is possible that torso-like is older than this (indeed, we have only examined a single myriapod genome), it is not present in multiple chelicerate genomes, implying it did not evolve in the common ancestor of arthropods (Figs 4, S3, Data S5).…”

Gene Content Evolution in the Arthropods

“…We combined these newly sequenced genomes with those of 48 previously sequenced arthropods creating a dataset comprising 76 species representing the four extant arthropod subphyla and spanning 21 taxonomic orders. Using the OrthoDB gene orthology database 7 , we annotated 38,195 protein ortholog groups (orthogroups/gene families) among all 76 species (Fig. 1).…”

“…This phylogeny is mostly consistent with previous arthropod phylogenies [8][9][10] , with the exception being that we recover a monophyletic Crustacea, rather than the generally accepted paraphyletic nature of Crustacea in respect to Hexapoda, the difference likely due to our restricted taxon sampling (see Methods). We reconstructed the gene content and protein domain arrangements for all 38,195 orthogroups in each of the lineages for the 76 species in the arthropod phylogeny. This resource (available at https://i5k.gitlab.io/ArthroFam/ and Table S11) forms the basis for the analyses detailed below and is an unprecedented tool for identifying and tracking genomic changes over arthropod evolutionary history.…”

“…The i5K pilot initiative has assembled an unparalleled genomic dataset for arthropods research and conducted a detailed phylogenetic analysis of evolutionary changes at the genomic level within this diverse and fascinating phylum. The combined research output of species-level i5K work has been substantial and wide-ranging, addressing pests of agricultural crops 32,33 and animals 34 , urban 20,35 and forest 36 pests, biocontrol species 37 , along with developmental models 18,38,39 , indicators of water quality and models for toxicology 15,40 (Table S1).…”