Transcriptome-based Phylogeny of the Semi-aquatic Bugs (Hemiptera: Heteroptera: Gerromorpha) Reveals Patterns of Lineage Expansion in a Series of New Adaptive Zones

Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France / Evolutionary Biology, Department of Ecology and Genetics, Uppsala University, SE-752 36 Uppsala, Sweden.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Biodiversidade Entomológica,. Rio de Janeiro, RJ, Brasil.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France / Department of Ecology and Evolutionary Biology, University of Toronto, M5S 3B2 Toronto, Ontario, Canada.
Center for Scientific Computing (sciCORE), University of Basel, 4056 Basel, Switzerland.
Department of Zoology, University of Cambridge, Downing St Cambridge, CB2 3EJ Cambridge, UK.
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
Departamento de Genética y Biología Molecular, Universidad de Panamá, Estafeta Universitaria, Panamá, Panamá.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Biodiversidade Entomológica. Rio de Janeiro, RJ, Brasil.
Department of Natural Sciences, Bishop Museum, 1525 Bernice St., Honolulu 96817, HI, USA.
School of Life Sciences, Sun Yat-sen University, 135 Xingangxi Road, Guangzhou 510275, Guangdong, People’s Republic of China.
Department of Ecology and Evolutionary Biology, University of Toronto, M5S 3B2 Toronto, Ontario, Canada.
Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Biodiversidade Entomológica. Rio de Janeiro, RJ, Brasil.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon1, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5242, Ecole Normale Supérieure de Lyon, 69007 Lyon, France / Evolutionary Biology, Department of Ecology and Genetics, Uppsala University, SE-752 36 Uppsala, Sweden.

Abstract

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, innovations have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. Water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a monophyletic lineage of insects that transitioned to live on the water–air interface and that 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 on the water surfaces. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

Keywords in Portuguese

Adaptação
Adaptação, zona adaptável
Gerromorpha
Chave de inovação
Filogenia
Insetos semi-aquáticos

Keywords

Adaptation
Adaptation, adaptive zone
Gerromorpha
Key innovation
Phylogeny
Semi-aquatic bugs

Publisher

Oxford University Press

Citation

ARMISÉN, David et al. Transcriptome-based Phylogeny of the Semi-aquatic Bugs (Hemiptera: Heteroptera: Gerromorpha) Reveals Patterns of Lineage Expansion in a Series of New Adaptive Zones. Mol. Biol. Evol., v. 39, n. 11, p. 1 - 19, Oct. 2022.

DOI

10.1093/molbev/msac229

ISSN

0737-4038

Please use this identifier to cite or link to this item: https://www.arca.fiocruz.br/handle/icict/55823

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Copyright

Open access

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