“Evolution of genetic variance during adaptive radiation”

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Greg M. Walter, J. David Aguirre, Mark W. Blows, and Daniel Ortiz-Barrientos (Apr 2018)

The DOI will be http://dx.doi.org/10.1086/696123

Natural selection increases genetic variance in the direction of natural selection to facilitate adaptive radiation

The evolution of genetic variance during adaptive radiation

Adaptive radiation occurs when new forms adapt rapidly to novel environments. Natural selection can favor certain combinations of traits, but not all trait combinations are possible. For example, the genes controlling plant height can also determine plant width and create a strong genetic correlation where wider plants are also taller, while short wide plants are never observed. Natural selection should then occur in directions determined by the availability of genetic variance, along the genetic correlation. However, if natural selection favors a trait combination that is not accessible because it lies away from this genetic correlation (i.e., short, wide plant shapes), adaptation towards this optimal phenotype would be difficult. Genetic correlations between traits are therefore expected to restrict the rate of adaptation because they are not expected to align with the optimal phenotype after the colonization of a novel habitat, making it difficult to understand how adaptive radiation occurs.

Walter et al. estimated genetic correlations between ten morphological traits for four contrasting ecotypes of an Australian wildflower that displays strong morphological divergence. The authors show that genetic correlations among traits are different in each ecotype, suggesting that genetic correlations are malleable during the early stages of adaptive radiation. Divergence in genetic correlations was associated with divergence in traits, indicating that in each environment adaptation occurred along trait combinations that possessed the greatest genetic variance. One possibility is that radiations proceed because natural selection strengthens beneficial genetic correlations at the expense of other trait combinations. Alternatively, rare alleles present in the ancestral population may become beneficial in a novel environment and rapidly rise in frequency. Both scenarios could align genetic correlations with the optimal phenotype, ultimately suggesting that during the early stages of adaptive radiation, natural selection can focus genetic variation in the direction of selection and promote rapid adaptive divergence.


Abstract

Genetic correlations between traits can concentrate genetic variance into fewer phenotypic dimensions that can bias evolutionary trajectories along the axis of greatest genetic variance and away from optimal phenotypes, constraining the rate of evolution. If genetic correlations limit adaptation, rapid adaptive divergence between multiple contrasting environments may be difficult. However, if natural selection increases the frequency of rare alleles after colonization of new environments, an increase in genetic variance in the direction of selection can accelerate adaptive divergence. Here, we explored adaptive divergence of an Australian native wildflower by examining the alignment between divergence in phenotype mean and divergence in genetic variance among four contrasting ecotypes. We found divergence in mean multivariate phenotype along two major axes represented by different combinations of plant architecture and leaf traits. Ecotypes also showed divergence in the level of genetic variance in individual traits, and the multivariate distribution of genetic variance among traits. Divergence in multivariate phenotypic mean aligned with divergence in genetic variance, with much of the divergence in phenotype among ecotypes associated with changes in trait combinations containing substantial levels of genetic variance. Overall, our results suggest that natural selection can alter the distribution of genetic variance underlying phenotypic traits, increasing the amount of genetic variance in the direction of natural selection and potentially facilitating rapid adaptive divergence during an adaptive radiation.