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Adaptive evolution is a well-appreciated process that can sustain or rescue populations facing strong selection gradients [ — ]. Yet several criteria must be met before local adaptation can be confirmed. Our results are consistent with the expectations of the first two criteria, but we are not yet able to deduce whether there is a genetic basis for such changes.

Phenotypic plasticity defined here as the ability to modulate phenotype in response to environmental cues can also produce phenotypes that appear different and adaptive, yet may be genetically indistinguishable from other populations [ — ]. Because plasticity can promote adaptation, inhibit adaptation, or be the adaptive response itself, uncovering the role of phenotypic plasticity remains one of the most important challenges for understanding and predicting adaptive responses to climate change [ 31 — 34 , , — ].

Indeed, some degree of phenotypic plasticity has been observed in nearly every trait that has been measured to date, which underlines the importance of examining the contribution of plasticity in studies of adaptive responses [ 32 — 34 , , — ]. Maternal effects induced by environmental conditions experienced by the parents are also emerging as important factors that influence offspring fitness in different environments [ , ]. The divergent responses that we present in this paper may be the production of either maternal effects, phenotypic plasticity, or local adaptation alone.

However, some blend of these mechanisms is more likely. For example, exposure to saltwater during the ontogeny of coastal individuals may have initiated cascades of plastic responses that predisposed females from coastal populations toward salt tolerant responses. These responses may have transferred to offspring, which mixes plasticity with maternal effects. Alternatively, coastal individuals with increased ability to tolerate salt through enhanced plasticity may have been favored by selection. Presumably, selecting for more plastic individuals would gradually increase the overall amount of plasticity observed in coastal populations, which blends plasticity with genetic adaptation sensu Baldwin effect [ ].

In reality, there are a multitude of possible mechanistic combinations as plasticity, local adaptation, and maternal effects can be reciprocal processes that serve as both the product and raw material for selection and adaptation. Future research should prioritize discerning how adaptive evolution, phenotypic plasticity, and maternal effects are interwoven to produce different responses to environmental stressors especially in organisms with complex life cycles.

A more complete understanding of all contributing processes will help managers identify thresholds of tolerance, detect vulnerable populations, and determine which organisms are likely to successfully tolerate novel stressors and persist in their environments. Despite the consistent differences in behavior, embryo, and larval survivorship we observed between inland and coastal populations, our results indicate that all populations and life stages of Hyla cinerea coastal and inland populations are salt-sensitive.

Frog pairs laid the majority of eggs into freshwater in all populations; saltwater negatively affected hatching rates across all populations, and saltwater reduced survivorship for both coastal and inland tadpoles. While we have focused on the degree to which these responses differed among populations as indications of adaptive responses, we believe that it should be noted that anurans on the whole, remain an osmotically sensitive group of organisms even in chronically salt-exposed populations.

The continued preference for, and higher performance in, freshwater, even among coastal populations, may indicate that thresholds of saltwater tolerance exist. This study provides the following insights: First, our meta-analysis offers a quantitative baseline for salt tolerance in anurans and provides important context for future field observations and experimental studies exploring saltwater tolerance in anurans.

The meta-analysis also shows that generally, anurans are salt-sensitive across species and across life stages and are therefore likely to be adversely affected by progressive salinization of freshwater systems. Second, we show different sensitivities and responses to salt stress across life stages and across populations, significant information for future studies and management. Third, we provide initial evidence that despite their sensitivity, some anuran species Hyla cinerea have populations that are able to respond adaptively to salt stress across different life stages.

Though these findings are an encouraging indication that some frog populations may persist through salinization, our results also illuminate that much more remains to be known. Key unknowns include the physiological mechanisms and adaptive processes that underlie salt tolerance in anurans, determining whether we can expect adaptive responses to match the pace and intensity of environmental change i. Testing multiple mechanistic hypotheses about adaptive processes e. Yet identifying populations with complex life cycles that demonstrate divergent responses to an environmental stressor across life stages such as coastal frog populations adapting to saline environments may provide unique and valuable opportunities to empirically address questions about the etiology of adaptive and non-adaptive responses, how novel adaptive phenotypes emerge, and how population and demographic dynamics interact with adaptive processes.

We thank members of McCoy lab group, K. McCoy, A. Stuckert, and J. Touchon for their thoughtful insights during the development of this work. We also extend thanks to A. McFarland and C. Thaxton for field and laboratory assistance. MAA carried out experimentation and data extraction. Both authors read and approved the final manuscript. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material. Molly A. Albecker, Email: ude. Michael W. McCoy, Email: ude. National Center for Biotechnology Information , U. Journal List Front Zool v. Front Zool. Published online Aug 1. Albecker and Michael W. Author information Article notes Copyright and License information Disclaimer. Corresponding author. Received Mar 15; Accepted Jul This article has been cited by other articles in PMC. Associated Data Supplementary Materials Additional file 1: Detailed list of studies included in the meta-analysis. Abstract Background In many regions, freshwater wetlands are increasing in salinity at rates exceeding historic levels.

Results Meta-analysis revealed differential vulnerability to salt stress across life stages with the egg stage as the most salt-sensitive. Conclusions Collectively, our data suggest that some species of anuran amphibians have divergent and adaptive responses to salt exposure across populations and across different life stages. Electronic supplementary material The online version of this article doi Keywords: Secondary salinization, Anuran amphibian, Sea level rise, Saltwater tolerance, Climate change, Complex life history.

Background Accumulating greenhouse gas concentrations are increasing the energy retained in the atmosphere, which is in turn causing global mean sea levels to rise through intensified ice sheet and glacier melting and thermal expansion of ocean water [ 1 — 4 ]. Meta-analysis Literature search We searched Google Scholar and Scopus databases for experimental studies evaluating the survivorship of anuran amphibians after experimental exposure to saltwater.

Data extraction After refining our database to studies, each study was read in detail and data were extracted from the text or figures. Field survey Study sites We monitored wetlands regularly to make sure species that breed at different times could be detected. Survey techniques We used standard sampling methods to characterize anuran presence and relative abundance including auditory call surveys, standardized dip netting for larvae, and active searching for adults [ 72 , 73 ].

Common garden experiments We used Hyla cinerea , the American green tree frog average size: 3. Oviposition site choice and egg hatching We tested oviposition site choice by collecting four amplexed pairs of Hyla cinerea from either coastal or inland populations. Tadpole survivorship To determine the effects of salinity on tadpole survival, we utilized the individuals hatched from eggs laid in freshwater during the previous oviposition experiments. Meta-analysis To estimate the probability of survival in saltwater for each life stage across anuran taxa and across salinities, we tested how increasing salinity affects anuran survivorship across clades for each life stage e.

Field survey We utilized the posterior distribution from the meta-analysis of all anuran species to predict the probability of anuran survivorship across several salinities including the salinities where we observed coastal Hyla cinerea during field surveys.

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Tadpole survivorship To quantify how salinity, location, and time e. Results Meta-analysis Effects of salt on amphibian survivorship We utilized data from 39 papers published between to early see Additional file 1 for detailed information. Open in a separate window. Table 1 The location and identity of the four anuran species observed in coastal, salt-invaded wetlands along with the highest salinity in which each species was observed.

Relative abundance In general, we noted that relative abundances of all species except Hyla cinerea declined as wetlands grew more saline. Probability of field findings Using the posterior probability distributions from our meta-analysis we examined the relative probability of finding frogs in the observed salinities: 3. Table 2 Predicted survivorship and Bayesian Credible Intervals of anurans in various salinities based on the findings of the meta-analysis Fig.

Common garden experiments The oviposition site choice experiment utilized Hyla cinerea pairs collected from three geographically discrete populations from inland and coastal locations in eastern North Carolina. Oviposition site choice We conducted four replicates in coastal and inland locations.

Egg hatching Salinity and source population affect the probability that any eggs would hatch out of a particular treatment Fig. Tadpole survivorship The predicted survival probability for coastal and inland Hyla cinerea tadpoles following a 6-day acclimation to freshwater 0. Discussion We are at the precipice of dramatic environmental transformation as a result of global climate change, which provides the ideal canvas for exploring organismal responses to environmental change.

Meta-analysis and field surveys Studies on amphibian responses to saltwater often begin with some variant of the statement, it is well accepted that frogs do not belong in saline habitats. Common garden experiments In the oviposition, hatching, and tadpole survivorship experiments, we find evidence for altered and adaptive responses to salinization across multiple life stages in Hyla cinerea.

Conclusions This study provides the following insights: First, our meta-analysis offers a quantitative baseline for salt tolerance in anurans and provides important context for future field observations and experimental studies exploring saltwater tolerance in anurans. Additional files Additional file 1: K, csv Detailed list of studies included in the meta-analysis.

Additional file 2: Table S1. Acknowledgements We thank members of McCoy lab group, K. Availability of data and materials We intend to make our code and data freely available in a public database upon publication. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interest. Footnotes Electronic supplementary material The online version of this article doi Contributor Information Molly A. References 1. How much more climate change and sea level rise?

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