Synergistic innovations enabled the radiation of anglerfishes in the deep open ocean

Major ecological transitions are thought to fuel diversification, but whether they are contingent on the evolution of certain traits called key innovations1Miller A.H. Stroud J.T. Losos J.B. The ecology and evolution of key innovations.Trends Ecol. Evol. 2023; 38: 122-131https://doi.org/10.1016/j.tree.2022.09.005Abstract Full Text Full Text PDF Scopus (13) Google Scholar is unclear. Key innovations are routinely invoked to explain how lineages rapidly exploit new ecological opportunities.1Miller A.H. Stroud J.T. Losos J.B. The ecology and evolution of key innovations.Trends Ecol. Evol. 2023; 38: 122-131https://doi.org/10.1016/j.tree.2022.09.005Abstract Full Text Full Text PDF Scopus (13) Google Scholar,2Stroud J.T. Losos J.B. Ecological Opportunity and Adaptive Radiation.Annu. Rev. Ecol. Evol. Syst. 2016; 47: 507-532https://doi.org/10.1146/annurev-ecolsys-121415-032254Crossref Scopus (317) Google Scholar,3Gavrilets S. Losos J.B. Adaptive Radiation: Contrasting Theory with Data.Science. 2009; 323: 732-737https://doi.org/10.1126/science.1157966Crossref PubMed Scopus (526) Google Scholar However, investigations of key innovations often focus on single traits rather than considering trait combinations that collectively produce effects of interest.4Donoghue M.J. Sanderson M.J. Confluence, synnovation, and depauperons in plant diversification.New Phytol. 2015; 207: 260-274https://doi.org/10.1111/nph.13367Crossref PubMed Scopus (158) Google Scholar Here, we investigate the evolution of synergistic trait interactions in anglerfishes, which include one of the most species-rich vertebrate clades in the bathypelagic, or "midnight," zone of the deep sea: Ceratioidea.5Pietsch T.W. Oceanic Anglerfishes: Extraordinary Diversity in the Deep Sea.1st ed. University of California Press, 2009Crossref Google Scholar Ceratioids are the only vertebrates that possess sexual parasitism, wherein males temporarily attach or permanently fuse to females to mate.6Pietsch T.W. Dimorphism, Parasitism and Sex: Reproductive Strategies among Deepsea Ceratioid Anglerfishes.Copeia. 1976; 1976: 781-793https://doi.org/10.2307/1443462Crossref Google Scholar,7Pietsch T.W. Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes).Ichthyol. Res. 2005; 52: 207-236https://doi.org/10.1007/s10228-005-0286-2Crossref Scopus (83) Google Scholar We show that the rapid transition of ancestrally benthic anglerfishes into pelagic habitats occurred during a period of major global warming 50–35 million years ago.8Westerhold T. Marwan N. Drury A.J. Liebrand D. Agnini C. Anagnostou E. Barnet J.S.K. Bohaty S.M. De Vleeschouwer D. Florindo F. et al.An astronomically dated record of Earth's climate and its predictability over the last 66 million years.Science. 2020; 369: 1383-1387https://doi.org/10.1126/science.aba6853Crossref PubMed Google Scholar,9Meckler A.N. Sexton P.F. Piasecki A.M. Leutert T.J. Marquardt J. Ziegler M. Agterhuis T. Lourens L.J. Rae J.W.B. Barnet J. et al.Cenozoic evolution of deep ocean temperature from clumped isotope thermometry.Science. 2022; 377: 86-90https://doi.org/10.1126/science.abk0604Crossref Scopus (33) Google Scholar This transition coincided with the origins of sexual parasitism, which is thought to increase the probability of successful reproduction once a mate is found in the midnight zone, Earth's largest habitat.5Pietsch T.W. Oceanic Anglerfishes: Extraordinary Diversity in the Deep Sea.1st ed. University of California Press, 2009Crossref Google Scholar,6Pietsch T.W. Dimorphism, Parasitism and Sex: Reproductive Strategies among Deepsea Ceratioid Anglerfishes.Copeia. 1976; 1976: 781-793https://doi.org/10.2307/1443462Crossref Google Scholar,7Pietsch T.W. Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes).Ichthyol. Res. 2005; 52: 207-236https://doi.org/10.1007/s10228-005-0286-2Crossref Scopus (83) Google Scholar Our reconstruction of the evolutionary history of anglerfishes and the loss of immune genes support that permanently fusing clades have convergently degenerated their adaptive immunity. We find that degenerate adaptive immune genes and sexual body size dimorphism, both variably present in anglerfishes outside the ceratioid radiation, likely promoted their transition into the bathypelagic zone. These results show how traits from separate physiological, morphological, and reproductive systems can interact synergistically to drive major transitions and subsequent diversification in novel environments.