Plasticity in nonsense-mediated decay and translation initiation regulate polyphenism

Developmental plasticity is increasingly recognised as facilitator of evolutionary novelty. However, how plasticity itself evolves and how variation in plastic trait expression is structured in populations remain unknown1,2. The predatory nematode Pristionchus pacificus exhibits mouth-form plasticity with underlying molecular mechanisms being increasingly identified3. We investigate the temporal scale of natural variation of mouth-form plasticity. An 11-year survey characterised Adoretus beetle-derived isolates from Colorado, La Reunion Island and revealed a gradual shift in mouth-form preference. Quantitative trait locus mapping of mouth-form preferences identified a single peak harbouring the developmental switch gene eud-1. Through CRISPR-engineering and biochemical assays, we show that plasticity in nonsense-mediated decay coupled with alternative start codon selection resulting in different N-terminal proteoforms of EUD-1 are associated with natural variation of mouth-form preference. This work provides molecular explanations for variation in plastic trait expression and links nonsense variants in the major developmental switch locus to ecological and evolutionary processes.