Environmental effects on genetic variance are likely to constrain adaptation in novel environments

Author:

Walter Greg M12,Monro Keyne2,Terranova Delia3,la Spina Enrico4,Majorana Maria4,Pepe Giuseppe4,Clark James15,Cozzolino Salvatore3,Cristaudo Antonia4,Hiscock Simon J5,Bridle Jon16

Affiliation:

1. School of Biological Sciences, University of Bristol , Bristol , United Kingdom

2. School of Biological Sciences, Monash University , Melbourne , Australia

3. Department of Biology, University of Naples Federico II , Naples , Italy

4. Department of Biological, Geological and Environmental Sciences, University of Catania , Catania , Italy

5. Department of Biology, University of Oxford , Oxford , United Kingdom

6. Department of Genetics, Evolution and Environment, University College London , London , United Kingdom

Abstract

Abstract Adaptive plasticity allows populations to cope with environmental variation but is expected to fail as conditions become unfamiliar. In novel conditions, populations may instead rely on rapid adaptation to increase fitness and avoid extinction. Adaptation should be fastest when both plasticity and selection occur in directions of the multivariate phenotype that contain abundant genetic variation. However, tests of this prediction from field experiments are rare. Here, we quantify how additive genetic variance in a multivariate phenotype changes across an elevational gradient, and test whether plasticity and selection align with genetic variation. We do so using two closely related, but ecologically distinct, sister species of Sicilian daisy (Senecio, Asteraceae) adapted to high and low elevations on Mt. Etna. Using a quantitative genetic breeding design, we generated and then reciprocally planted c. 19,000 seeds of both species, across an elevational gradient spanning each species’ native elevation, and then quantified mortality and five leaf traits of emergent seedlings. We found that genetic variance in leaf traits changed more across elevations than between species. The high-elevation species at novel lower elevations showed changes in the distribution of genetic variance among the leaf traits, which reduced the amount of genetic variance in the directions of selection and the native phenotype. By contrast, the low-elevation species mainly showed changes in the amount of genetic variance at the novel high elevation, and genetic variance was concentrated in the direction of the native phenotype. For both species, leaf trait plasticity across elevations was in a direction of the multivariate phenotype that contained a moderate amount of genetic variance. Together, these data suggest that where plasticity is adaptive, selection on genetic variance for an initially plastic response could promote adaptation. However, large environmental effects on genetic variance are likely to reduce adaptive potential in novel environments.

Funder

Natural Environment Research Council

Australian Research Council

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

Reference63 articles.

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3. Climate change disrupts local adaptation and favours upslope migration;Anderson,2020

4. Patterns of phenotypic plasticity along a thermal gradient differ by trait type in an alpine plant;Arnold;Functional Ecology,2022

5. Predicting evolutionary rescue via evolving plasticity in stochastic environments;Ashander,2016

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