Abstract
SUMMARYA major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system.
Highlights
Mechanosensory neurons from trigeminal ganglia (TG) mediate the initial detection of the mechanical stimuli in the bill, tongue, and oral cavity and are essential for tactile-based foraging
We found that the abundance of neurons responding to mechanical stimulation varied significantly across duck species, from lowest in wood duck to highest in Pekin duck (33.7% and 68.8% of all TG neurons, respectively; c2 test; p < 0.0001) (Figures 1B and 1C)
Even in wood duck, the proportion of mechanoreceptors was higher than that found earlier in chicken (19.8% of all TG neurons), a strictly visually foraging bird (Schneider et al, 2017). These data show that the proportional expansion of mechanosensitive neurons in TG is a general phenomenon among Anatidae waterfowl, consistent with the idea that many duck species are tactilely guided foragers
Summary
Mechanosensory neurons from trigeminal ganglia (TG) mediate the initial detection of the mechanical stimuli in the bill, tongue, and oral cavity and are essential for tactile-based foraging. Ruddy ducks (Oxyura jamaicensis) are divers, feeding by straining benthic material underwater (Tome and Wrubleski, 1988). The Pekin duck (Anas platyrhynchos domesticus), a domesticated descendant of the mallard, and its close relative the black duck (Anas rubripes) are probably the most sophisticated tactile foragers and are the most well studied (Zweers, 1977). While it is difficult to compare physiological sensitivities to touch among the duck species directly, Pekin and black ducks are tactilely guided dabblers known to possess an exceptional ability to forage almost entirely based on the sense of touch. Some species are nocturnal foragers (black, mallard, ruddy, and scaup), while others are primarily diurnal (harlequin and merganser) or crepuscular (wood) (McNeil et al, 1992)
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