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

Authors: ARMISEN, DAVID - University Of Lyon; RAJAKUMAR, RAJENDHARAN - University Of Florida; FRIEDRICH, MARKUS - Wayne State University; BENOIT, JOSHUA - University Of Cincinnati; ROBERTSON, HUGH - University Of Illinois; PANFILIO, KRISTEN - University Of Cologne; AHN, SEUNG-JOON - Oregon State University; Poelchau, Monica; CHAO, HSU - Baylor College Of Medicine; DINH, HUYEN - Baylor College Of Medicine; DODDAPANENI, HARSHA VARDHAN - Baylor College Of Medicine; DUGAN, SHANNON - Baylor College Of Medicine; GIBBS, RICHARD - Baylor College Of Medicine; HUGHES, DANIEL S. - Baylor College Of Medicine; HAN, YI - Baylor College Of Medicine; LEE, SANDRA - Baylor College Of Medicine; MURALI, SHWETHA - University Of Washington; MUZNY, DONNA - Baylor College Of Medicine; QU, JIAXIN - Baylor College Of Medicine; WORLEY, KIM - Baylor College Of Medicine; MUNOZ-TORRES, MONICA - Lawrence Berkeley National Laboratory; ABOUHEIF, EHAB - McGill University - Canada; BONNETON, FRANCOIS - University Of Lyon; CHEN, TRAVIS - McGill University - Canada; Childers, Christopher; CRIDGE, ANDREW GRAHAM - Max Planck Institute Of Chemical Ecology; CRUMIERE, ANTONIN JEAN JO - University Of Lyon; DECARAS, AMELIE - University Of Lyon; DIDION, ELISE - University Of Cincinnati; DUNCAN, ELIZABETH - University Of Otago; ELPIDINA, ELENA - Moscow State University; FAVE, MARIE-JULIE - McGill University - Canada; FINET, CEDRIC - University Of Lyon; JACOBS, CHRIS G. - Leiden University; JARVELA, ALYS - University Of Maryland; JENNINGS, EMILY - University Of Cincinnati; JONES, JEFFERY - Wayne State University; LESOWAY, MARYNA - Smithsonian Tropical Research; LOVEGROVE, MACKENZIE - University Of Otago; MARTYNOV, ALEXANDER - Skolkovo Institute Of Science And Technology; Oppert, Brenda; LILLICO-OUACHOUR, ANGELICA - University Of Leeds; RAJAKUMAR, ARJUNA - University Of Leeds; REFKI, PETER NAGUI - Max Planck Institute For Evolutionary Biology; ROSENDALE, ANDREW - University Of Cincinnati; SANTOS, MARIA EMILIA - University Of Lyon; TOUBIANA, WILLIAM - University Of Lyon; VAN DER ZEE, MAURIJN - Leiden University; VARGAS JENTZSCH, IRIS - University Of Cologne; LOWMAN, AIDAMALIA - University Of Lyon; VIALA, SEVERINE - University Of Lyon; RICHARDS, STEPHEN - Baylor College Of Medicine; KHILA, ABDERRAHMAN - University Of Lyon

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2018
Publication Date: 11/21/2018
Citation: Armisen, D., Rajakumar, R., Friedrich, M., Benoit, J.B., Robertson, H.M., Panfilio, K.A., Ahn, S., Poelchau, M.F., Chao, H., Dinh, H., Doddapaneni, H., Dugan, S., Gibbs, R.A., Hughes, D.T., Han, Y., Lee, S.L., Murali, S.C., Muzny, D.M., Qu, J., Worley, K.C., Munoz-Torres, M., Abouheif, E., Bonneton, F., Chen, T., Chiang, L.-M., Childers, C., Cridge, A., Crumiere, A.J., Decaras, A., Didion, E.M., Duncan, E.J., Elpidina, E.N., Fave, M., Finet, C., Jacobs, C.C., Jarvela, A., Jennings, E.C., Jones, J.W., Lesoway, M.P., Lovegrove, M.R., Martynov, A., Oppert, B.S., Lillico-Ouachour, A., Rajakumar, A., Refki, P., Rosendale, A.J., Santos, M., Toubiana, W., van der Zee, M., Vargas Jentzsch, I.M., Lowman, A.V., Viala, S., Richards, S., Khila, A. 2018. The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water. BMC Genomics. 19:832. https://doi.org/10.1186/s12864-018-5163-2.
DOI: https://doi.org/10.1186/s12864-018-5163-2

Interpretive Summary: Water striders have a unique capability to walk on water and have been studied from the standpoint of their ecology and biology. To fully understand the genetics responsible for their adaptation to living on water surfaces, the water strider genome was sequenced and assembled, and genes from the assembly were annotated manually. Expansions of gene families associated with growth, vision, and other critical life processes were found that can explain the adaptation of this insect to occupy a unique ecological niche. These data will enable the coupling of water strider biology with underlying genetic architecture and enhanced appreciation for the factors that contribute to the success of these insects as dwellers of the water surface.

Technical Abstract: Water striders conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they 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 thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi genome, the first water strider genome to be sequenced so far. Gerris buenoi genome is about 1000Mb and the sequencing effort recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the Gerris genome includes three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway in water striders. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the Gerris buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.