Concerted genetic and transcriptomic shifts underlie adaptation to a latitudinal thermal gradient within a widespread mantis shrimp

Widely dispersed species are often found across heterogeneous environments, which can result in localized adaptive divergence among populations. While previous studies have highlighted the role of gene sequence variation in shaping adaptive divergence patterns, the contribution of gene expression changes remains poorly characterized. We explore this in a widespread mantis shrimp (Oratosquilla oratoria), distributed along the well-defined thermal clines in the Northwestern Pacific (NWP), to dissect the interplay between sequence and expression variation in adaptation to a latitudinal thermal gradient. Population transcriptomics of 51 O. oratoria individuals from four populations along the NWP latitudinal gradient revealed a significant north–south population structure at both the sequence and expression levels. The absence of isolation by distance underscored the role of natural selection. Positive correlations between nucleotide diversity and expression diversity within and among populations suggest that genetic and expression variation collaboratively enhance O. oratoria’ s survival in diverse habitats. By integrating with knowledge of gene functions from a reverse ecology perspective, we identified an over-representation of temperature-relevant candidate gene transcripts (CGTs) contributing significantly to the expression divergence among O. oratoria populations, whereas no such over-representation was observed in highly divergent CGTs across different latitudinal populations. Compared to the gene set, the differentially expressed and highly divergent CGTs exhibit greater overlap in functional categories, including the biological process and molecular function GO terms. Our findings demonstrate that local thermal selection may have acted on gene expression levels, thereby prompting further investigation into potential non-coding regulatory changes. Additionally, the functional consistency of differentially-expressed and highly divergent CGTs compared to a shared gene set implies alternative ways for O. oratoria to respond to thermally environmental stresses across latitudes. This work provides evidence of how gene sequence and expression changes work in concert in a widespread species in response to a highly selective environment.