Paralog switching facilitates euryhalinity: Ontogenetic,
microevolutionary and macroevolutionary evidence
Abstract
Euryhalinity is present in diverse aquatic taxa and requires flexible
osmoregulation to field the challenges posed by differing salinities.
Na+, K+-ATPase (NKA) is a ubiquitous
ion pump in the gills of fishes and, for some species, paralogs of the
catalytic α-subunit (NKA α1a and α1b) exhibit reciprocal expression
between fresh- and seawater, termed paralog-switching. We investigated
the expression and evolution of NKA paralogs in Alewife (Alosa
pseudoharengus), a euryhaline and migratory fish. Comparisons between
landlocked and diadromous life history forms and migrant and pre-migrant
ontogenetic stages were used to study shifts in NKA paralog expression
related to freshwater or seawater specialization. We exposed juvenile
diadromous and landlocked alewives to freshwater (0 ppt) and seawater
(30 ppt) for 2, 5, and 15 days. Additionally, we sampled migrant and
pre-migrant alewives from the natal freshwater environment or after 24
hours in seawater. Diadromous Alewife exhibited salinity-dependent
paralog switching, and the freshwater-specialized landlocked life
history form showed greater upregulation of NKA α1b in seawater. Migrant
Alewife showed a loss of freshwater readiness traded for seawater
specialization through greater reliance (via upregulation) on NKA α1a in
freshwater. Molecular phylogenies show Alewife NKA paralogs originated
independently of paralogs in salmonids and other members of
Euteleosteomorpha. This study demonstrated that NKA paralog switching is
tied to halohabitat profile and that duplications of the ancestral NKA
gene provided the substrate for multiple, independent molecular
solutions for supporting a diadromous life history.