Rapid evolution of genome-wide gene expression and plasticity during
saline to freshwater invasions by the copepod Eurytemora affinis
Saline migrants into freshwater habitats constitute among the most
destructive invaders in aquatic ecosystems throughout the globe.
However, evolutionary and physiological mechanisms underlying such
habitat transitions remain poorly understood. To explore mechanisms of
freshwater adaptation and distinguish between adaptive (evolutionary)
and acclimatory (plastic) responses to salinity change, we examined
genome-wide patterns of gene expression between ancestral saline and
derived freshwater populations of the Eurytemora affinis species
complex, reared under two different common-garden conditions (0 vs. 15
PSU). We found that evolutionary shifts in gene expression (between
saline and freshwater inbred lines) showed far greater changes and were
more widespread than acclimatory responses to salinity (0 vs. 15 PSU).
Most notably, many genes showing evolutionary shifts in gene expression
across the salinity boundary were associated with ion transport
function, with inorganic cation transmembrane transport forming the
largest Gene Ontology category. Of particular interest was the sodium
transporter, the Na+/H+ antiporter
(NHA) gene family, which was discovered in animals relatively recently.
A few key ion regulatory genes, such as NHA paralog #7, demonstrated
concordant evolutionary and plastic shifts in gene expression,
suggesting the evolution of ion transporter plasticity and function
during rapid invasions into novel salinities. Moreover, freshwater
invasions were associated with the evolution of reduced plasticity in
the freshwater population, again for the same key ion transporters,
consistent with the predicted evolution of canalization following
adaptation to stressful conditions. Our results have important
implications for understanding invasion mechanisms by some of the most
widespread invaders in aquatic habitats.