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

Abstract

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.

Keywords: Adaptation; Evolution; Genome sequence; Water striders; Water surface locomotion.

Fig. 1

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). b G. 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

Fig. 2

Orthology comparison between Gerris buenoi and other arthropod species. Genome proteins were clustered with proteins of other 12 arthropod species based on OrthoDB orthology

Fig. 3

Characterization of the three copies of the Insulin Receptor in Gerris buenoi. a Protein domain comparison between the three InRs of G. buenoi and the Human InR. b InR phylogenetic relationship amongst Insecta. Branch support numbers at branches. A non-circular version included in Additional file 1: Figure S1. c Simplified Arthropoda phylogeny based on [115] depicting InR duplications and loss events

Fig. 4

Genomic locus and global analysis of the Gerris buenoi opsin gene repertoire. a Structure of the scaffold containing the four G. buenoi long wavelength (LWS) opsins. b Retinal opsin repertoires of key hemipteran species and reconstructed opsin subfamily loss and expansion events along the hemipteran phylogeny. c Comparison of amino acid residues at the four tuning sites identified in the LWS opsins of Lepidoptera [68, 69]. Site numbers based on [68]. Numbers in parentheses are experimentally determined sensitivity maxima. Species abbreviations: Amel = Apis mellifera, Dmel = Drosophila melanogaster, Gbue = Gerris buenoi, Gbim = Gryllus bimaculatus, Larc = Limenitis archippus, Lart = Limenitis arthemis astyanax

Fig. 5

Phylogenetic analysis of four different Clans of the cytochrome P450s of Gerris buenoi with other insect species. a Clan 2, b Clan mitochondria, c Clan 3, and d Clan 4. The G. buenoi sequences are indicated in red and bold