Fine‐grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of nonrandom gene flow in restricting effective migration among wetlands

Abstract

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.

Compensating for delayed hatching reduces offspring immune response and increases life‐history costs

“…While the effects of early metamorphosis on fitness are not ubiquitous (perhaps due to smaller number of studies; Earl and Whiteman ), they are likely to be important in time‐constrained systems. In our study system, the duration of the larval period is likely to have important fitness effects as suggested by the strong adaptive divergence in this trait among local Rana arvalis demes (Richter‐Boix et al , ). It is possible that the effect was especially clear in the present study as the tadpoles were challenged at the end of larval period, leaving them little time to compensate by (further) accelerating development.…”

Phenotypic divergence of the common toad (Bufo bufo) along an altitudinal gradient: evidence for local adaptation

“…In the case of common toads, the breeding habitat choice in altitude could be limited because lowland ponds probably are beyond the migration distance. A powerful approach to disentangle these processes is to investigate this correlation at a local scale where the selective agent is not correlated with geographic distances, preventing IBD within the area (Richter-Boix et al, 2013).…”

“…We estimated the predicted sample variance for Q ST of a neutral trait by simulating it with information on F ST (using neutral markers) and the within-population additive variance for the trait analyzed. Using the R-script provided by Richter-Boix et al (2013) and developed by Lind et al (2011), we tested whether the (Q ST -F ST ) of each trait differed from the neutral expectations. To estimate significance, we calculated the expected among-population variance component for a neutral trait using the observed values of F ST and the withinpopulation variance (see Equation (4) in Lind et al, 2011).…”

“…The difference between both statistics (Q ST -F ST ) was simulated 50 000 times to create a distribution of neutral trait to compare the observed Q ST -F ST. Giving that F ST using neutral markers should be similar to Q ST for a neutral trait, Q ST -F ST can be used as a test statistic, where the observed Q ST -F ST difference is compared with the 95% distribution of the simulated (Q ST -F ST ) values (Lind et al, 2011;Richter-Boix et al, 2013).…”

Multifarious selection through environmental change: acidity and predator-mediated adaptive divergence in the moor frog (Rana arvalis)

“…[10]) and partly explain the strong local adaptation found in amphibian metapopulations (e.g. [29,52,53]). For the case here, selection against immigrant genotypes from neutral ponds may be strong in acidic ponds because of their low embryonic acid stress tolerance and high risk of predation during the larval stage [32].…”