Independent and adaptive evolution of phenotypic novelties driven by coral symbiosis in barnacle larvae

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The invasion of novel habitats is recognized as a major promotor of adaptive trait evolution in animals. We tested whether similar ecological niches entail independent and adaptive evolution of key phenotypic structures related to larval host invasion in distantly related taxa. We use disparately related clades of coral barnacles as our model system (Acrothoracica: Berndtia and Thoracicalcarea: Pyrgomatidae). We analyze the larval antennular phenotypes and functional morphologies facilitating host invasion. Extensive video recordings show that coral host invasion is carried out exclusively by cypris larvae with spear-shaped antennules. These first exercise a series of complex probing behaviors followed by repeated antennular penetration of the soft host tissues, which subsequently facilitates permanent invasion. Phylogenetic mapping of larval form and function related to niche invasion in 99 species of barnacles (Thecostraca) compellingly shows that the spear phenotype is uniquely associated with corals and penetrative behaviors. These features evolved independently in the two coral barnacle clades and from ancestors with fundamentally different antennular phenotypes. The larval host invasion system in coral barnacles likely evolved adaptively across millions of years for overcoming challenges associated with invading and entering demanding coral hosts.

Udgave nummer1
Sider (fra-til)139-157
Antal sider19
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
This work was supported by a double degree graduate grant from the Natural History Museum of Denmark (SNM) and the Taiwan International Graduate Program (TIGP) to ND, a Villum Experiment Grant to JO and a grants from the Carlsbserg Foundation and the Danish Agency for Independent Research (FNU) to JTH. GAK was financially suported by the Russian Foundation for Basic Research (grant MNT_a 21‐54‐52003). BKKC is supported by the Senior Investigator Award (Academia Sinica) and Ministry of Science and Technology (109‐2811‐B‐001 ‐536 ‐).

Funding Information:
We thank members of the Coastal Ecology Lab at Academia Sinica including P. C. Tsai, Y. F. Tsao, W. P. Hsieh, and D. Eibye‐Jacobsen (Natural History Museum of Denmark) for assistance with collection and culturing. The authors thank Dr. C. Nielsen (Natural History Museum of Denmark), E. Krichilsky (American Museum of Natural History and Columbia University, USA), R. B. Dahl (Academia Sinica, Taiwan), and F. M. G. de Mattos (Academia Sinica, Taiwan) for their useful critique on the manuscript and the photographic material. Four referees and editors Dr. M. Zelditch (Museum of Palaeontology, University of Michigan, USA) and Dr. J.‐P. Huang (Academia Sinica, Taiwan) provided exceptionally rewarding reviews of earlier versions of the manuscript. The entire editorial team is thanked for being extremely helpful and encouraging during the entire submission process. ND acknowledges relentless support from the Taiwan International Graduate Program (TIGP‐BIODIV), the Natural History Museum of Denmark. Support to JO and JTH to collect y‐larvae was supported by The Villum Experiment. The authors dedicate this manuscript to Dr. R. Strathmann (University of Washington, USA) for his seminal and inspiring works on invertebrate larval biology and evolution.

Publisher Copyright:
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.

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