The functional diversification of somatosensory neuron repertoires across Mammalia

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Abstract
The striking diversity of mammalian body forms and surfaces, lifestyles, and habitats prompts the question of how each species’ somatosensory neuron repertoire accommodates such diversity. The visual and olfactory systems diversify by gaining and losing sensor/receptor genes and corresponding sensory cell types. Using multiomic single-cell analysis of dorsal root ganglia neurons from thirteen different mammalian species and cross-species functional studies enabled by cell-type-specific enhancer viruses, we show that mammals instead assemble species-specific, functionally distinct somatosensory neuron repertoires from a conserved set of neuron types (orthotypes). Repertoire diversification takes multiple forms: orthotype abundance scales with variable bodily traits like hair follicle density, facilitating relevant behaviors; sensor/receptor expression is shuffled across species, such that orthotypes can detect different stimuli in different species; and orthotypes split into functionally distinct, species-specific subtypes (paratypes). Thus, unlike other sensory systems, the mammalian somatosensory system diversifies through multifarious changes to conserved orthotypes, enabling adaptation to diverse habitats, lifestyles, and body forms.
Funding Information
  • National Institutes of Health (NS129589)
  • National Institutes of Health (NS146561)
  • National Institutes of Health (NS143029)
  • National Institutes of Health (NS132196)
  • National Institutes of Health (NS097344)
  • National Institutes of Health (NS119476)
  • National Science Foundation (CBET-2011619)
  • the Hock E. Tan and K. Lisa Yang Center for Autism Research
  • The Burroughs Wellcome Fund
  • The Rita Allen Foundation
  • The K. Lisa Yang Brain Body Center at Harvard Medical School
  • The Edward R. and Anne G. Lefler Center for Neurodegenerative Disorders

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