Abstract
Signals of natural selection can be quickly eroded in high gene-flow
systems, curtailing efforts to understand how and when genetic
adaptation occurs in the ocean. This long-standing, unresolved topic in
ecology and evolution has renewed importance because changing
environmental conditions are driving range expansions that may
necessitate rapid evolutionary responses. One example occurs in Kellet’s
whelk (Kelletia kelletii), a common subtidal gastropod with a
~ 40-60 day pelagic larval duration that expanded their
biogeographic range northward in the 1970s by over 300 kilometers. To
test for genetic adaptation, we performed a series of experimental
crosses with Kellet’s whelk adults collected from their historical (HxH)
and recently expanded range (ExE), and conducted RNA-Seq on offspring
that we reared in a common garden environment. We identified 2,770
differentially expressed genes (DEGs) between 54 offspring samples with
either only historical-range (HxH offspring) or expanded-range (ExE
offspring) ancestry. Using SNPs called directly from the DEGs, we
assigned samples of known origin back to their range of origin with
unprecedented accuracy for a marine species (92.6 and 94.5% for HxH and
ExE offspring, respectively). The SNP with the highest predictive
importance occurred on triosephosphate isomerase (TPI), an essential
metabolic enzyme involved in cold stress response. TPI was significantly
upregulated and contained a non-synonymous mutation in the expanded
range. Our findings pave the way for accurately identifying patterns of
dispersal, gene flow, and population connectivity in the ocean by
demonstrating that experimental transcriptomics can reveal mechanisms
for how marine organisms respond to changing environmental conditions.