Experimental evidence that phenotypic evolution but not plasticity occurs along genetic lines of least resistance in homogeneous environments

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Abstract

Genetic correlations concentrate genetic variation in certain directions of the multivariate phenotype. Adaptation and, under some models, plasticity is expected to occur in the direction of the phenotype containing the greatest amount of genetic variation (gmax). However, this may hinge upon environmental heterogeneity, which can affect patterns of genetic variation. I use experimental evolution to test whether plasticity and phenotypic evolution follow gmax during adaptation to environments that varied in environmental heterogeneity. For >25 generations, Drosophila melanogaster populations were exposed to six homogeneous or spatially and temporally heterogeneous treatments involving hot (25ºC) and cold (16ºC) temperatures. Five wing traits were assayed in both temperatures. Wing morphology diverged between populations evolving in homogeneous hot and cold temperatures in a direction of the phenotype containing a large proportion of genetic variance, and that aligned closely with gmax at 16ºC, but not 25ºC. Spatial heterogeneity produced an intermediate phenotype, which was associated with similar genetic variance across assay temperatures compared to all other treatments. Surprisingly, plasticity across assay temperatures evolved in a different direction to phenotypic evolution and aligned better with maternal variance than gmax. Together, these results provide experimental evidence for evolution along genetic lines of least resistance in homogeneous environments, but no support for predicting plastic responses from the orientation of genetic variation. These results also suggest that spatial heterogeneity could maintain genetic variation that increases the stability of genetic variance across environments.
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Abstract

Genetic correlations concentrate genetic variation in certain directions of the multivariate phenotype. Adaptation and, under some models, plasticity is expected to occur in the direction of the phenotype containing the greatest amount of genetic variation (gmax). However, this may hinge upon environmental heterogeneity, which can affect patterns of genetic variation. I use experimental evolution to test whether plasticity and phenotypic evolution follow gmax during adaptation to environments that varied in environmental heterogeneity. For >25 generations, Drosophila melanogaster populations were exposed to six homogeneous or spatially and temporally heterogeneous treatments involving hot (25ºC) and cold (16ºC) temperatures. Five wing traits were assayed in both temperatures. Wing morphology diverged between populations evolving in homogeneous hot and cold temperatures in a direction of the phenotype containing a large proportion of genetic variance, and that aligned closely with gmax at 16ºC, but not 25ºC. Spatial heterogeneity produced an intermediate phenotype, which was associated with similar genetic variance across assay temperatures compared to all other treatments. Surprisingly, plasticity across assay temperatures evolved in a different direction to phenotypic evolution and aligned better with maternal variance than gmax. Together, these results provide experimental evidence for evolution along genetic lines of least resistance in homogeneous environments, but no support for predicting plastic responses from the orientation of genetic variation. These results also suggest that spatial heterogeneity could maintain genetic variation that increases the stability of genetic variance across environments. DOI https://doi.org/10.32942/X2HW54 Subjects Ecology and Evolutionary Biology, Life Sciences

Keywords

adaptation, additive genetic variance, environmental heterogeneity, Experimental Evolution, G-matrix, wing shape, additive genetic variance, environmental heterogeneity, Experimental evolution, g-matrix, wing shape Dates Published: 2024-08-12 13:02 Last Updated: 2024-08-12 17:02 License CC BY Attribution 4.0 International Additional Metadata Data and Code Availability Statement: Data are located in the Dryad Digital Repository (https:// doi.org/10.5061/dryad.1719; Yeaman et al. 2010) and also accompany the R code on Zenodo (https://doi.org/10.5281/zenodo.7160306). Language: English

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