Mosaic phenotypic evolution underlies the adaptive success of water-surface colonization in Gerromorpha
Abstract
Understanding how the remarkable phenotypic diversity observed in organisms arises through shifts in macroevolutionary patterns and tempos is a fundamental challenge in evolutionary biology. Phenotypes often evolve in a mosaic pattern during adaptive transitions. For organisms that have invaded highly specialized habitats, such as the unique two-phase interface habitats (water surfaces), the macroevolutionary history of their phenotypic diversification remains only superficially understood. Semiaquatic bugs (Insecta: Heteroptera: Gerromorpha), which exhibit extensive habitat diversification and unparalleled phenotypic innovation, represent one of the most successful extant adaptive groups at this interface and provide an excellent system for study. By analyzing their adaptive transitions and phenotypic macroevolutionary history, we demonstrate that Gerromorpha experienced a single major adaptive transition from land to the water surface. Subsequently, semiaquatic bugs successfully colonized a wide range of distinct water-surface habitats. During this process, phenotypic space was explored under strong constraints and along pronounced mosaic trajectories; i.e., different body regions exhibited markedly distinct patterns of phenotypic space occupation and partitioning, as well as markedly different evolutionary rates. Furthermore, we showed that this mosaic pattern of phenotypic space occupation and rates of exploration had complex and critical effects on the invasion and colonization of water-surface habitats. Our study provides a typical case of macroevolutionary dynamics in species adapted to specialized air–water interface habitats, emphasizing the complex and significant roles of environmental context and functional demands in shaping patterns of phenotypic evolution.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (24)
Zezhong Jin
Institute of Entomology, College of Life Sciences, Nankai University
Mu Qiao
Siying Fu
Institute of Entomology, College of Life Sciences, Nankai University
Zihe Li
Institute of Entomology, College of Life Sciences, Nankai University
Boxiong Guo
Institute of Entomology, College of Life Sciences, Nankai University
Hongjiao Li
Institute of Entomology, College of Life Sciences, Nankai University
Zhaoqi Leng
Institute of Entomology, College of Life Sciences, Nankai University
Matthew R. Pintar
Institute of Environment, Florida International University
Jakob Damgaard
Natural History Museum of Denmark, Zoological Museum
Benjamin L. Makepeace
Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool
Silvia A. Mazzucconi
Laboratorio de Entomología, Instituto de Biodiversidad y Biología Experimental y Aplicada, Consejo Nacional de Investigaciones Científicas y Técnicas - Universidad de Buenos Aires, Departamento de Biodiversidad y Biología Experimental - Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires
Gavril Marius Berchi
Department of Biology, Faculty of Chemistry, Biology, Geography, West University of Timișoara
Fabio Cianferoni
Research Institute on Terrestrial Ecosystems, National Research Council of Italy
Dan A. Polhemus
Department of Natural Sciences, Bishop Museum
Kohei Watanabe
Ishikawa Insect Museum
Jun Nakajima
Seraphine Esemu
Laboratory for Emerging Infectious Diseases, Faculty of Science, University of Buea
Chen Liu
Beichen Zhang
Institute of Entomology, College of Life Sciences, Nankai University
Huanhuan Yang
School of Bioengineering, Qilu University of Technology (Shandong Academy of Sciences)
Shujing Wang
Institute of Entomology, College of Life Sciences, Nankai University
Huaijun Xue
Institute of Entomology, College of Life Sciences, Nankai University
Wenjun Bu
Institute of Entomology, College of Life Sciences, Nankai University
Zhen Ye