Molecular mechanisms of local adaptation for salt‐tolerance in a treefrog

Salinization is a global phenomenon affecting ecosystems and forcing freshwater organisms to deal with increasing levels of ionic stress. However, our understanding of mechanisms that permit salt tolerance in amphibians is limited. This study investigates mechanisms of salt tolerance in locally adapted, coastal populations of a treefrog, Hyla cinerea. Using a common garden experiment, we (i) determine the extent that environment (i.e., embryonic and larval saltwater exposure) or genotype (i.e., coastal vs. inland) affects developmental benchmarks and transcriptome expression, and (ii) identify genes that may underpin differences in saltwater tolerance. Differences in gene expression, survival, and plasma osmolality were most strongly associated with genotype. Population genetic analyses on expressed genes also delineated coastal and inland groups based on genetic similarity. Coastal populations differentially expressed osmoregulatory genes including ion transporters (atp1b1, atp6V1g2, slc26a), cellular adhesion components (cdh26, cldn1, gjb3, ocln), and cytoskeletal components (odc1‐a, tgm3). Several of these genes are the same genes expressed by euryhaline fish after exposure to freshwater, which is a novel finding for North American amphibians and suggests that these genes may be associated with local salinity adaptation. Coastal populations also highly expressed glycerol‐3‐phosphate dehydrogenase 1 (gpd1), which indicates they use glycerol as a compatible osmolyte to reduce water loss – another mechanism of saltwater tolerance previously unknown in frogs. These data signify that Hyla cinerea inhabiting coastal, brackish wetlands have evolved a salt‐tolerant ecotype, and highlights novel candidate pathways that can lead to salt tolerance in freshwater organisms facing habitat salinization.

• Publication year

  2021

• Venue

  Molecular Ecology

• Publication date

  2021-03-02

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1111/mec.15867PMID 33655636
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Local adaptation for enhanced salt tolerance reduces non‐adaptive plasticity caused by osmotic stress

  2019influential reference
• Enhanced salt tolerance of euryhaline tadpoles depends on increased Na+, K+-ATPase expression after salinity acclimation.

  2019influential reference
• Comparative Analysis of Anuran Amphibian Skin Microbiomes Across Inland and Coastal Wetlands

  2018cited by this paper
• Contaminant exposure effects in a changing climate: how multiple stressors can multiply exposure effects in the amphipod Hyalella azteca

  2018cited by this paper
• The cryoprotectant system of Cope’s gray treefrog, Dryophytes chrysoscelis: responses to cold acclimation, freezing, and thawing

  2018cited by this paper
• A Review of the Combined Threats of Road Salts and Heavy Metals to Freshwater Systems

  2018cited by this paper
• Freshwater salinization syndrome on a continental scale

  2018cited by this paper
• Exploring the effects of salinization on trophic diversity in freshwater ecosystems: a quantitative review

  2018cited by this paper
• Advancing Understanding of Amphibian Evolution, Ecology, Behavior, and Conservation with Massively Parallel Sequencing

  2018cited by this paper
• Integrative Population and Physiological Genomics Reveals Mechanisms of Adaptation in Killifish

  2018cited by this paper
• Overexpression of Glycerol-3-Phosphate Acyltransferase from Suaeda salsa Improves Salt Tolerance in Arabidopsis

  2017cited by this paper
• Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults

  2017cited by this paper
• Evaluating hypotheses of expansion from refugia through comparative phylogeography of south‐eastern Coastal Plain amphibians

  2017cited by this paper
• The Oyster River Protocol: a multi-assembler and kmer approach for de novo transcriptome assembly

  2017cited by this paper
• Adaptive responses to salinity stress across multiple life stages in anuran amphibians

  2017influential reference
• Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats

  2017cited by this paper
• vcfr: a package to manipulate and visualize variant call format data in R

  2017cited by this paper
• Molecular Physiology of Freeze Tolerance in Vertebrates.

  2017cited by this paper
• Adapting to a Changing Environment: Modeling the Interaction of Directional Selection and Plasticity.

  2016cited by this paper
• Near-optimal probabilistic RNA-seq quantification

  2016influential reference
• Data-driven hypothesis weighting increases detection power in genome-scale multiple testing

  2016cited by this paper
• Differential analysis of RNA-seq incorporating quantification uncertainty

  2016cited by this paper
• Abiotic and biotic constraints across reptile and amphibian ranges

  2016cited by this paper
• Molecular Machinery for Vasotocin-Dependent Transepithelial Water Movement in Amphibians: Aquaporins and Evolution

  2015influential reference
• TransRate: reference-free quality assessment of de novo transcriptome assemblies

  2015cited by this paper
• A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands

  2015cited by this paper
• BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs

  2015cited by this paper
• Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads

  2015cited by this paper
• Assessment of the coordinated role of ST3GAL3, ST3GAL4 and ST3GAL6 on the α2,3 sialylation linkage of mammalian glycoproteins.

  2015cited by this paper
• Transcriptomes reveal the genetic mechanisms underlying ionic regulatory adaptations to salt in the crab-eating frog

  2015cited by this paper
• Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

  2015cited by this paper
• Occurrence of Amphibians in Saline Habitats: A Review and Evolutionary Perspective

  2015cited by this paper
• Past and future sea-level rise along the coast of North Carolina, USA

  2014cited by this paper
• Climate change, adaptation, and phenotypic plasticity: the problem and the evidence

  2014cited by this paper
• Novel vasotocin-regulated aquaporins expressed in the ventral skin of semiaquatic anuran amphibians: evolution of cutaneous water-absorbing mechanisms.

  2014cited by this paper
• Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

  2014cited by this paper
• Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus

  2014cited by this paper
• Effects of Salinity and Pesticide on Sperm Activity and Oviposition Site Selection in Green Treefrogs, Hyla cinerea

  2014cited by this paper
• A Review of the Effects of Altered Hydrology and Salinity on Vertebrate Fauna and Their Habitats in Northeastern Florida Bay

  2014cited by this paper
• Salinity acclimation enhances salinity tolerance in tadpoles living in brackish water through increased Na⁺ , K⁺ -ATPase expression.

  2014cited by this paper
• Gene expression and localization of two types of AQP5 in Xenopus tropicalis under hydration and dehydration.

  2014cited by this paper
• R: A language and environment for statistical computing.

  2014influential reference
• Do the same genes underlie parallel phenotypic divergence in different Littorina saxatilis populations?

  2014cited by this paper
• Fast and sensitive protein alignment using DIAMOND

  2014influential reference
• Second-generation PLINK: rising to the challenge of larger and richer datasets

  2014influential reference
• Influence of artificial channels on the source and extent of saline water intrusion in the wind tide dominated wetlands of the southern Albemarle estuarine system (USA)

  2014cited by this paper
• Trimmomatic: a flexible trimmer for Illumina sequence data

  2014influential reference
• The Future of Species Under Climate Change: Resilience or Decline?

  2013cited by this paper
• Effects of salinity stress on Bufo balearicus and Bufo bufo tadpoles: Tolerance, morphological gill alterations and Na(+)/K(+)-ATPase localization.

  2013cited by this paper
• On the optimal trimming of high-throughput mRNA sequence data

  2013influential reference
• Cytoplasmic 5′-3′ exonuclease Xrn1p is also a genome-wide transcription factor in yeast

  2013cited by this paper
• Evolutionary rescue from extinction is contingent on a lower rate of environmental change

  2013cited by this paper
• Lethal and Sublethal Effects of Salinity on Three Common Texas Amphibians

  2013cited by this paper
• Altered expression of Na(+)/K(+)-ATPase and other osmoregulatory genes in the gills of euryhaline animals in response to salinity transfer: a meta-analysis of 59 quantitative PCR studies over 10 years.

  2013cited by this paper
• Variation in Salinity Tolerance among Larval Anurans: Implications for Community Composition and the Spread of an Invasive, Non-native Species

  2013cited by this paper
• Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change

  2013cited by this paper
• SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing

  2012influential reference
• Effect size estimation.

  2012cited by this paper
• Road to evolution? Local adaptation to road adjacency in an amphibian (Ambystoma maculatum)

  2012cited by this paper
• Salinity Acclimation Affects Survival and Metamorphosis of Crab-eating Frog Tadpoles

  2012cited by this paper
• Global Scale Variation in the Salinity Sensitivity of Riverine Macroinvertebrates: Eastern Australia, France, Israel and South Africa

  2012cited by this paper
• CD-HIT: accelerated for clustering the next-generation sequencing data

  2012cited by this paper
• Quantitative assessment on the cloning efficiencies of lentiviral transfer vectors with a unique clone site

  2012cited by this paper
• Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation

  2012influential reference
• Tight junctions, tight junction proteins and paracellular permeability across the gill epithelium of fishes: a review.

  2012cited by this paper
• Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

  2011cited by this paper
• Transcriptomic responses to salinity stress in invasive and native blue mussels (genus Mytilus)

  2011cited by this paper
• Recent ecological responses to climate change support predictions of high extinction risk

  2011cited by this paper
• Functional genomics of physiological plasticity and local adaptation in killifish.

  2011cited by this paper
• Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data

  2011influential reference
• Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms.

  2011cited by this paper
• PUMPING IONS: RAPID PARALLEL EVOLUTION OF IONIC REGULATION FOLLOWING HABITAT INVASIONS

  2011cited by this paper
• Additive threats from pathogens, climate and land-use change for global amphibian diversity

  2011cited by this paper
• A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data

  2011cited by this paper
• Sequence analysis Advance Access publication June 7, 2011 The variant call format and VCFtools

  2010influential reference
• De novo assembly and analysis of RNA-seq data

  2010cited by this paper
• Lethal and Sublethal Effects of Embryonic and Larval Exposure of Hyla versicolor to Stormwater Pond Sediments

  2010cited by this paper
• Polyamines and abiotic stress tolerance in plants

  2010cited by this paper
• Water adaptation strategy in anuran amphibians: molecular diversity of aquaporin.

  2010cited by this paper
• Expression and immunolocalization of aquaporins HC-1, -2, and -3 in Cope's gray treefrog, Hyla chrysoscelis.

  2010cited by this paper
• Effect of road deicing salt on the susceptibility of amphibian embryos to infection by water molds.

  2009cited by this paper
• Structuring and extracting knowledge for the support of hypothesis generation in molecular biology

  2009cited by this paper
• Fast model-based estimation of ancestry in unrelated individuals.

  2009influential reference
• Physiology and function of the tight junction.

  2009cited by this paper
• Molecular and cellular regulation of water homeostasis in anuran amphibians by aquaporins.

  2009cited by this paper
• Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity.

  2009cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009influential reference
• adegenet: a R package for the multivariate analysis of genetic markers

  2008cited by this paper
• Adaptation as a potential response to sea-level rise: a genetic basis for salinity tolerance in populations of a coastal marsh fish

  2008cited by this paper
• BMC Bioinformatics BioMed Central

  2008cited by this paper
• Consequences of Climate Change on the Ecogeomorphology of Coastal Wetlands

  2008cited by this paper
• Intracellular Organic Osmolytes: Function and Regulation*

  2008cited by this paper
• Osmotic and Ionic Regulation : Cells and Animals

  2008cited by this paper
• WGCNA: an R package for weighted correlation network analysis

  2008cited by this paper
• Maternal effects and evolution at ecological time‐scales

  2007cited by this paper
• Amphibian aquaporins and adaptation to terrestrial environments: a review.

  2007cited by this paper
• Water relations of tetrapod integument

  2006cited by this paper
• Hormonal regulation of ion and water transport in anuran amphibians.

  2006cited by this paper
• Identification of a mitochondrial ATP synthase small subunit gene (RMtATP6) expressed in response to salts and osmotic stresses in rice (Oryza sativa L.).

  2006cited by this paper
• Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica).

  2006cited by this paper

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• Insights into molecular and biochemical approaches of multi-stress responses to horticultural crops

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• Genetic Adaptation to Brackish Water and Spawning Season in European Cisco

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  2024cites this paper
• Genome-wide comparative analyses highlights selection signatures underlying saline adaptation in Chilika buffalo.

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  2023cites this paper
• Population genomics analysis to identify ion and water transporter genes involved in the adaptation of Tibetan naked carps to brackish water.

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  2022cites this paper
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• Relationship between anuran larvae occurrence and aquatic environment in septentrional east Palearctic landscapes

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  2020cites this paper