Evolution of novel sensory organs in fish with legs

Affiliations
  • 1Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
  • 2Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.
  • 3Max Planck Institute for Biological Intelligence, 82319 Seewiesen, Germany.
  • 4Roger Williams University, Bristol, RI 02809, USA.
  • 5Department of Civil, Chemical and Environmental Engineering, University of Genoa, 16145 Genoa, Italy.
  • 6Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA. Electronic address: kingsley@stanford.edu.
  • 7Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: nbellono@harvard.edu.

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Abstract

How do animals evolve new traits? Sea robins are fish that possess specialized leg-like appendages used to “walk” along the sea floor. Here, we show that legs are bona fide sense organs that localize buried prey. Legs are covered in sensory papillae that receive dense innervation from touch-sensitive neurons, express non-canonical epithelial taste receptors, and mediate chemical sensitivity that drives predatory digging behavior. A combination of developmental analyses, crosses between species with and without papillae, and interspecies comparisons of sea robins from around the world demonstrate that papillae represent a key evolutionary innovation associated with behavioral niche expansion on the sea floor. These discoveries provide unique insight into how molecular-, cellular-, and tissue-scale adaptations integrate to produce novel organismic traits and behavior.

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