Predicting the biodiversity impacts of global warming implies that we know where and with what magnitude these impacts will be encountered. Amphibians are currently the most threatened vertebrates, mainly due to habitat loss and to emerging infectious diseases. Global warming may further exacerbate their decline in the near future, although the impact might vary geographically. We predicted that subtropical amphibians should be relatively susceptible to warming-induced extinctions because their upper critical thermal limits (CT max ) might be only slightly higher than maximum pond temperatures (T max ). We tested this prediction by measuring CT max and T max for 47 larval amphibian species from two thermally distinct subtropical communities (the warm community of the Gran Chaco and the cool community of Atlantic Forest, northern Argentina), as well as from one European temperate community. Upper thermal tolerances of tadpoles were positively correlated (controlling for phylogeny) with maximum pond temperatures, although the slope was steeper in subtropical than in temperate species. CT max values were lowest in temperate species and highest in the subtropical warm community, which paradoxically, had very low warming tolerance (CT max -T max ) and therefore may be prone to future local extinction from acute thermal stress if rising pond T max soon exceeds their CT max . Canopy-protected subtropical cool species have larger warming tolerance and thus should be less impacted by peak temperatures. Temperate species are relatively secure to warming impacts, except for late breeders with low thermal tolerance, which may be exposed to physiological thermal stress in the coming years.
Anurans breed in a variety of aquatic habitats with contrasting levels of desiccation risk, which may result in selection for faster development during larval stages. Previous studies suggest that species in ephemeral ponds reduce their developmental times to minimize desiccation risks, although it is not clear how variation in desiccation risk affects developmental strategies in different species. Employing a comparative phylogenetic approach including data from published and unpublished studies encompassing 62 observations across 30 species, we tested if species breeding in ephemeral ponds (High risk) develop faster than those from permanent ponds (Low risk) and/or show increased developmental plasticity in response to drying conditions. Our analyses support shorter developmental times in High risk, primarily by decreasing body mass at metamorphosis. Plasticity in developmental times was small and did not differ between groups. However, accelerated development in High risk species generally resulted in reduced sizes at metamorphosis, while some Low risk species were able compensate this effect by increasing mean growth rates. Taken together, our results suggest that plastic responses in species breeding in ephemeral ponds are constrained by a general trade-off between development and growth rates.
In organisms with complex life cycles, environmentally induced plasticity across sequential stages can have important consequences on morphology and life history traits such as developmental and growth rates. However, previous research in amphibians and other ectothermic vertebrates suggests that some morphological traits are generally insensitive to environmental inductions. We conducted a literature survey to examine the allometric responses in relative hind leg length and head shape of post-metamorphic anuran amphibians to induced environmental (temperature, resource level, predation and desiccation risk) variation operating during the larval phase in 44 studies using 19 species. To estimate and compare plastic responses across studies, we employed both an index of plasticity and effect sizes from a meta-analysis. We found contrasting trait responses to different environmental cues. Higher temperatures increased development more than growth rate and induced smaller heads but not overall shifts in hind leg length. In contrast, an increment in resource availability increased growth more than development, with a parallel increase in hind leg length but no change in head shape. Increases in predation risk decreased both development and growth rates and slightly reduced relative hind leg length, but there was no change in head shape. Pond desiccation induced quick development and low growth rates, with no changes in morphology. Across environments, both hind leg and head shape plasticity were positively correlated with growth rate plasticity. However, plasticity of developmental rate was only correlated with head shape plasticity. Overall, these results suggest that environmental trends predicted by global warming projections, such as increasing pond temperature and accelerating pond desiccation, will significantly influence hind leg and head morphology in metamorphic frogs, which may affect performance and, ultimately, fitness.
In ectotherms, variation in life history traits among populations is common and suggests local adaptation. However, geographic variation itself is not a proof for local adaptation, as genetic drift and gene flow may also shape patterns of quantitative variation. We studied local and regional variation in means and phenotypic plasticity of larval life history traits in the common frog Rana temporaria using six populations from central Sweden, breeding in either open-canopy or partially closed-canopy ponds. To separate local adaptation from genetic drift, we compared differentiation in quantitative genetic traits (Q(ST)) obtained from a common garden experiment with differentiation in presumably neutral microsatellite markers (F(ST)). We found that R. temporaria populations differ in means and plasticities of life history traits in different temperatures at local, and in F(ST) at regional scale. Comparisons of differentiation in quantitative traits and in molecular markers suggested that natural selection was responsible for the divergence in growth and development rates as well as in temperature-induced plasticity, indicating local adaptation. However, at low temperature, the role of genetic drift could not be separated from selection. Phenotypes were correlated with forest canopy closure, but not with geographical or genetic distance. These results indicate that local adaptation can evolve in the presence of ongoing gene flow among the populations, and that natural selection is strong in this system.
Adaptive ecological differentiation among sympatric populations is promoted by environmental heterogeneity, strong local selection and restricted gene flow. High gene flow, on the other hand, is expected to homogenize genetic variation among populations and therefore prevent local adaptation. Understanding how local adaptation can persist at the spatial scale at which gene flow occurs has remained an elusive goal, especially for wild vertebrate populations. Here, we explore the roles of natural selection and nonrandom gene flow (isolation by breeding time and habitat choice) in restricting effective migration among local populations and promoting generalized genetic barriers to neutral gene flow. We examined these processes in a network of 17 breeding ponds of the moor frog Rana arvalis, by combining environmental field data, a common garden experiment and data on variation in neutral microsatellite loci and in a thyroid hormone receptor (TRβ) gene putatively under selection. We illustrate the connection between genotype, phenotype and habitat variation and demonstrate that the strong differences in larval life history traits observed in the common garden experiment can result from adaptation to local pond characteristics. Remarkably, we found that haplotype variation in the TRβ gene contributes to variation in larval development time and growth rate, indicating that polymorphism in the TRβ gene is linked with the phenotypic variation among the environments. Genetic distance in neutral markers was correlated with differences in breeding time and environmental differences among the ponds, but not with geographical distance. These results demonstrate that while our study area did not exceed the scale of gene flow, ecological barriers constrained gene flow among contrasting habitats. Our results highlight the roles of strong selection and nonrandom gene flow created by phenological variation and, possibly, habitat preferences, which together maintain genetic and phenotypic divergence at a fine-grained spatial scale.
One of the main questions in evolutionary and conservation biology is how geographical and environmental features of the landscape shape neutral and adaptive genetic variation in natural populations. The identification of genomic polymorphisms that account for adaptive variation can aid in finding candidate loci for local adaptation. Consequently, a comparison of spatial patterns in neutral markers and loci under selection may help disentangle the effects of gene flow, genetic drift and selection at the landscape scale. Many amphibians breed in wetlands, which differ in environmental conditions and in the degree of isolation, enhancing the potential for local adaptation. We used microsatellite markers to measure genetic differentiation among 17 local populations of Rana arvalis breeding in a network of wetlands. We found that locus RC08604 deviated from neutral expectations, suggesting that it is a good candidate for directional selection. We used a genetic network analysis to show that the allele distribution in this locus is correlated with habitat characteristics, whereas this was not the case at neutral markers that displayed a different allele distribution and population network in the study area. The graph approach illustrated the genomic heterogeneity (neutral loci vs. the candidate locus for directional selection) of gene exchange and genetic divergence among populations under directional selection. Limited gene flow between wetlands was only observed at the candidate genomic region under directional selection. RC08604 is partially located inside an up-regulated thyroid-hormone receptor (TRβ) gene coordinating the expression of other genes during metamorphosis and appears to be linked with variation in larval life-history traits found among R. arvalis populations. We suggest that directional selection on genes coding larval life-history traits is strong enough to maintain the divergence in these genomic regions, reducing the effective recombination of locally adapted alleles but not in other regions of the genome. Integrating this knowledge into conservation plans at the landscape scale will improve the design of management strategies to preserve adaptive genetic diversity in wetland networks.
The timing of seasonal life-history events is assumed to evolve to synchronize life cycles with the availability of resources. Temporal variation in breeding time can have severe fitness consequences for the offspring, but the interplay between adult reproductive decisions and offspring phenotypes remains poorly understood. Transgenerational plasticity (TGP) is a potential mechanism allowing rapid responses to environmental change. Here, we investigated if experimentally delayed breeding induces TGP in larval life-history traits in the moor frog (Rana arvalis). We found clear evidence of TGP in response to changes in breeding phenology: delayed breeding increased offspring development and growth rates in the absence of external cues. This constitutes the first unequivocal evidence for TGP in response to changes in breeding phenology in vertebrates. TGP can play an important role in adjusting offspring life-history strategies to the environment they are most likely to encounter, and may constitute an important mechanism for coping with climate change.
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