Unique genetic variants underlie parallel gene expression within a young adaptive radiation despite specialization on highly divergent resources

Abstract

Parallel evolution of gene expression commonly underlies convergent niche specialization, but parallel changes in expression could also underlie divergent specialization. We investigated divergence in gene expression and whole-genome genetic variation across three sympatric Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist and two derived specialists adapted to novel niches - a scale-eater and a snail-eater. We sampled total mRNA from all three species at two early developmental stages and compared gene expression with whole-genome genetic differentiation among all three species in 42 resequenced genomes. 80% of genes that were differentially expressed between snail-eaters and generalists were up or downregulated in the same direction between scale-eaters and generalists; however, there were no fixed variants shared between species underlying these parallel changes in expression. Genes showing parallel evolution of expression were enriched for effects on metabolic processes, whereas genes showing divergent expression were enriched for effects on cranial skeleton development and pigment biosynthesis, reflecting the most divergent phenotypes observed between specialist species. Our findings reveal that even divergent niche specialists may exhibit convergent adaptation to higher trophic levels through shared genetic pathways. This counterintuitive result suggests that parallel evolution in gene expression can accompany divergent ecological speciation during adaptive radiation.\n\nImpact SummaryAdaptations that result in unique forms of ecological specialization are central to research in evolutionary biology, yet little is known about their molecular foundations. We combined transcriptome sequencing with whole-genome divergence scans to study the molecular evolution of two specialist Cyprinodon pupfish species - a scale-eater and a snail-eater - that rapidly diverged from a sympatric generalist ancestor within the last 10,000 years. While parallel evolution of gene expression driving convergent niche specialization seems common, we present, to our knowledge, the first example of significant parallel changes in expression coinciding with divergent niche specialization. 80% of genes that were differentially expressed between snail-eaters and generalists showed the same direction of expression in scale-eaters relative to generalists. Furthermore, parallel evolution in expression seem to be controlled by unique genetic variants in each specialist species. Genes showing parallel changes in expression were enriched for metabolic processes that may facilitate adaptation to a higher trophic level, while genes showing divergent expression likely shape the striking morphological differences between specialists. These findings contribute to a more nuanced understanding of convergent adaptations that arise during speciation, and highlight how species can evolve similar expression profiles adapted to divergent niches.