Non-parallel transcriptional divergence during parallel adaptation

Mechanisms linking genotype to phenotype must simultaneously buffer organisms from developmental noise and allow for phenotypic plasticity in response to environmental cues. How mechanistic robustness and flexibility in biological systems bias evolution toward predictable outcomes remains an area of active debate. In this study, we leveraged phenotypic plasticity and parallel adaptation across independent lineages of Trinidadian guppies (Poecilia reticulata) to assess the predictability of transcriptional evolution during parallel adaptation. We observed substantial phenotypic plasticity in gene expression patterns as well as evolution of gene expression plasticity across populations. Although transcripts exhibiting expression plasticity within populations were more likely to differ in expression between populations, we found no consistent relationship between the direction of plasticity and evolutionary divergence. Similarly, while we found more overlap than expected by chance in genes differentially expressed between high- and low-predation populations from distinct lineages, the direction of expression divergence was uncoupled in the two drainages, and the majority of differentially expressed genes were not shared between lineages. Our data highlight transcriptional versatility associated with parallel phenotypic divergence in independent evolutionary lineages of a species known for rapid adaptation.