ABSTRACT
Environmentally induced plasticity in gene expression is one of the underlying mechanisms of adaptation to habitats with variable environments. For example, euryhaline crustaceans show predictable changes in the expression of ion-transporter genes during salinity transfers, although studies have typically been limited to specific genes, taxa and ecosystems of interest. Here, we investigated responses to salinity change at multiple organizational levels in five species of shrimp representing at least three independent invasions of the anchialine ecosystem, defined as habitats with marine and freshwater influences with spatial and temporal fluctuations in salinity. Although all five species were generally strong osmoregulators, salinity-induced changes in gill physiology and gene expression were highly species specific. While some species exhibited patterns similar to those of previously studied euryhaline crustaceans, instances of distinct and atypical patterns were recovered from closely related species. Species-specific patterns were found when examining: (1) numbers and identities of differentially expressed genes, (2) salinity-induced expression of genes predicted a priori to play a role in osmoregulation, and (3) salinity-induced expression of orthologs shared among all species. Notably, ion transport genes were unchanged in the atyid Halocaridina rubra while genes normally associated with vision and light perception were among those most highly upregulated. Potential reasons for species-specific patterns are discussed, including variation among anchialine habitats in salinity regimes and divergent evolution in anchialine taxa. Underexplored mechanisms of osmoregulation in crustaceans revealed here by the application of transcriptomic approaches to ecologically and taxonomically understudied systems are also explored.
FOOTNOTES
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: J.C.H., S.R.S.; Methodology: J.C.H., E.M., Y.F., R.P.H., S.R.S.; Formal analysis: J.C.H.; Investigation: J.C.H., E.M., Y.F., R.C.V.; Resources: Y.F., R.P.H., S.R.S.; Writing - original draft: J.C.H.; Writing - review & editing: J.C.H., E.M., Y.F., R.C.V., R.P.H., S.R.S.; Visualization: J.C.H.; Supervision: J.C.H., Y.F., R.P.H.; Project administration: J.C.H., E.M., Y.F., R.P.H., S.R.S.; Funding acquisition: J.C.H., S.R.S.
Funding
Funding was provided by the National Science Foundation (DEB0949855 to S.R.S., EPS 11-58862 to R.P.H., DEB1311500 and IIA1309694 to J.C.H.), the Japan Society for the Promotion of Science (SP13020 to J.C.H.) and the National Institutes of Health (F32GM116361 to J.C.H.). Deposited in PMC for release after 12 months.
Data availability
Transcriptomes are available from the Transcriptome Shotgun Assembly Sequence Database (NCBI TSA; accession numbers in Table S1 in figshare) and Dryad (Havird and Santos, 2014; doi:10.5061/dryad.jn8t1) while raw reads are available from the Sequence Read Archive (NCBI SRA; accession numbers in Table S2 in figshare). All datasets and supplementary figures/tables are available from the figshare repository (https://figshare.com/articles/Disparate_responses_to_salinity_across_species_and_organizational_levels_in_anchialine_shrimps/9976883).
- Received August 9, 2019.
- Accepted November 5, 2019.
- © 2019. Published by The Company of Biologists Ltd