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
innovations is unclear. Key innovations are routinely invoked to explain
how lineages rapidly exploit new ecological opportunities . However,
investigations of key innovations often focus on single traits rather than
considering trait combinations that collectively produce effects of
interest . 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. Ceratioids are the only vertebrates that possess sexual
parasitism, wherein males temporarily attach or permanently fuse to
females to mate. 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. 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. 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.