Environmentally-induced return to juvenile-like chemosensitivity in the respiratory control system of adult bullfrogs, Lithobates catesbeianus

An unanswered question in developmental physiology is to what extent does the environment vs. a genetic program produce phenotypes. Developing animals inhabit different environments and switch from one to another. Thus a developmental time course overlapping with environmental change confounds interpretations as to whether development (i.e., permanent processes) or environmental plasticity (i.e., reversible processes) generates phenotypes. Tadpoles of the American bullfrog, Lithobates catesbeianus, breathe water at early life-stages and minimally use lungs for gas exchange. As adults, bullfrogs rely on lungs for gas exchange, but spend months per year in ice-covered ponds without lung breathing. Aquatic-submergence, therefore, removes environmental pressures requiring lung breathing and enables separation of adulthood from environmental factors associated with adulthood that necessitate control of lung ventilation. To test the hypothesis that postmetamorphic respiratory control phenotypes arise through permanent developmental changes vs. reversible environmental signals, we measured respiratory-related nerve discharge in isolated brainstem preparations and action potential firing from CO₂-sensitive neurons in bullfrogs acclimatized to semi-terrestrial (air-breathing) and aquatic-overwintering (no air-breathing) habitats. We found that aquatic-overwintering significantly reduced neuroventilatory responses to CO₂ and O₂ involved in lung breathing. Strikingly, this gas sensitivity profile reflects that of water-breathing tadpoles. We further demonstrated that aquatic-overwintering reduced CO₂-induced firing responses of chemosensitive neurons. In contrast, respiratory rhythm generating processes remained adult-like after submergence. Our results establish that phenotypes associated with life-stage can arise from environmental plasticity per se. This provides evidence that developmental time courses coinciding with environmental changes obscure interpretations regarding origins of stage-dependent physiological phenotypes by masking plasticity.

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