Fine-scale genetic structure due to adaptive divergence among microhabitats

Abstract

It has been suggested that adaptive evolution on ecological timescales shapes communities. However, adaptation among environments relies on isolation or large selection coefficients that exceed migration effects. This reliance is tempered if adaptation is polygenic-does not depend on one allele completely replacing another but instead requires small allele frequency changes at many loci. Thus, whether individuals can evolve adaptation to fine-scale habitat variation (for example, microhabitats) is not resolved. Here we analyze the genetic divergence of the teleost fish, Fundulus heteroclitus, among microhabitats that are <200 m apart in three separate saltmarshes using 4741 single-nucleotide polymorphisms (SNPs). Among these SNPs, 1.3-2.3% have large and highly significant differences among microhabitats (mean F=0.15; false discovery rate ⩽1%). The divergence among microhabitats for these outlier SNPs is larger than that among populations, exceeds neutral expectation and indicates surprising population structure among microhabitats. Thus, we suggest that polygenic selection is surprisingly effective in altering allele frequencies among many different SNPs that share similar biological functions in response to environmental and ecological differences over very small geographic distances. We acknowledge the evolutionary difficulty of large genetic divergence among well-connected habitats. Therefore, these studies are only the first step to discern whether natural selection is responsible and capable of effecting genetic divergence on such a fine scale.

Spatial and phylogenetic structure of Alpine stonefly community assemblages across seven habitats using DNA-species

“…A high species turnover has been associated with poor dispersal abilities (Thompson & Townsend, 2006). We found a high replacement of the species by other species among habitats (species turnover = 0.60), suggesting that a non-random migration is likely to occur among habitats caused by environmental filtering or spatial restriction, which likely promote high diversity, as previously observed in the freshwater fish, Fecunduls heteroclitus (Wagner, Baris, Dayan, Du, Oleksiak, & Crawford, 2017). However, a high species turnover could also be associated with sampling bias.…”

Rapid polygenic selection generates fine spatial structure among ecological niches in a well-mixed population

“…Again, all SNPs that are significant at an FDR of 10% are also significant at the Bonferroni level and are hence displayed as the latter. Furthermore, pond:pond pairwise comparisons yield F ST outliers with similar magnitudes to basin:pond comparisons, contrary to the prior expectation of genetic divergence among distinct niches [11].…”

“…Contrary to the prediction that panmictic breeding every generation would inhibit local adaptation, previous work identified significant genetic divergence among F. heteroclitus inhabiting distinct niches less than 100m apart in three replicate estuaries/populations [11]. The authors identified single nucleotide polymorphisms (SNPs) displaying significant spatial differentiation among well-connected niches in each of three isolated estuaries and supported by three different selection tests.…”

“…Evolutionary adaptation on ecological scales is unlikely due to fundamental limits on the extent of selectively important allelic variation and the rate of adaptive change [7–10]. Yet, an increasing number of natural systems demonstrate adaptation on short temporal and small spatial scales [4]: significant divergence among demes associated with different ecological niches within a single population [11], a few generations of competition altering heritable toepad size and habitat use in anoles [12], repeated anthropogenic pollution resistance [13, 14], seasonal change in heritable thermal tolerance [15, 16], response to local anthropogenic heating [1,5,6], and other ecologically relevant traits [4,17–21]. These observations conflict with the predictions of classic population genetics, and their importance is hotly debated [22–26].…”

“…The authors identified single nucleotide polymorphisms (SNPs) displaying significant spatial differentiation among well-connected niches in each of three isolated estuaries and supported by three different selection tests. While none of the outlier loci were shared among all three replicate populations, many SNPs occur either: i) within the same gene at a different position, ii) in a duplicate gene or paralog, or iii) among genes with similar annotations or narrow, well-defined GO-terms [11]. That is, while no outlier SNPs were shared among the three replicate populations, there were signals of selection in the same gene or genes of similar function, a hallmark of redundancy.…”