Evolution of novel sensory organs in fish with legs
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Abstract
How do animals evolve new traits? Sea robins are unusual “walking” fishes that use leg-like appendages to navigate the seafloor. Here, we show that legs are bona fide sense organs that mediate the unique ability to localize and uncover buried prey. We then probe the developmental and physiological basis of these novel sense organs as a striking example of a major trait gain in evolution. We find certain sea robin species have legs with unique end-organs called papillae that mediate enhanced mechanical and chemical sensitivity to enable predatory digging behavior. Papillae exhibit dense innervation from touch-sensitive neurons, noncanonical epithelial taste receptors, and chemical sensitivity that drives predatory digging behavior. Using a combination of developmental analyses, crosses between species with and without papillae, and interspecies comparisons of sea robins from around the world, we demonstrate that papillae represent a key evolutionary innovation associated with behavioral niche expansion on the seafloor. These discoveries provide a conceptual framework for understanding how molecular, cellular, and tissue-scale adaptations integrate to produce novel organismic traits and behavior.
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We hypothesize that sea robins initially developed fin ray-like legs for locomotion. Ancestral organs then evolved limited sensory capability to facilitate manipulation of the visible substrate in search of food. Finally, evolution of sensory papillae further specialized legs to localize and uncover buried prey.
How much history/ecological data are there available for these species? It could be interesting to pair the phylogenetic patterns with other trait data to explicitly test different evolutionary hypotheses. e.g. is there a relationship with prey type? substrate? depth? biotic diversity?
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To test this ability, we developed a simple behavioral assay in which sea robins (Prionotus carolinus) were housed in a controlled tank with either mussels or capsules containing crude or filtered mussel extract buried in sand without visual cues (Fig. 1a, b, Supplementary movie 1). Sea robins alternated between short bouts of swimming and walking (Fig. 1b) and appeared to “scratch” at the sand surface with their legs while walking, which we hypothesized represented sensory behavior.
Do these behaviors vary at all as a function of what prey are used? I'm guessing you tested squid and crabs with P. carolinus as you did with P. evolans?
Presumably motile (squid/crabs) prey would give off a different set of cues that less/non-motile prey (mussels)? Specifically, I wonder if there is a tradeoff between chemo- and mechanosensation that is …
To test this ability, we developed a simple behavioral assay in which sea robins (Prionotus carolinus) were housed in a controlled tank with either mussels or capsules containing crude or filtered mussel extract buried in sand without visual cues (Fig. 1a, b, Supplementary movie 1). Sea robins alternated between short bouts of swimming and walking (Fig. 1b) and appeared to “scratch” at the sand surface with their legs while walking, which we hypothesized represented sensory behavior.
Do these behaviors vary at all as a function of what prey are used? I'm guessing you tested squid and crabs with P. carolinus as you did with P. evolans?
Presumably motile (squid/crabs) prey would give off a different set of cues that less/non-motile prey (mussels)? Specifically, I wonder if there is a tradeoff between chemo- and mechanosensation that is dependent on the amount of movement? Examining this relationship could be a potential route into the neural computations underlying digging behavior...
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