Evolvability and trait function predict phenotypic divergence of plant populations

Author:

Opedal Øystein H.1ORCID,Armbruster W. Scott23,Hansen Thomas F.4,Holstad Agnes5ORCID,Pélabon Christophe5ORCID,Andersson Stefan1ORCID,Campbell Diane R.6ORCID,Caruso Christina M.7ORCID,Delph Lynda F.8ORCID,Eckert Christopher G.9,Lankinen Åsa10,Walter Greg M.11ORCID,Ågren Jon12ORCID,Bolstad Geir H.13ORCID

Affiliation:

1. Department of Biology, Biodiversity Unit, Lund University, Lund 223 62, Sweden

2. School of Biological Sciences, University of Portsmouth, Portsmouth PO1 2DY, UK

3. Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775

4. Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo 0316, Norway

5. Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, Trondheim 7491, Norway

6. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697

7. Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada

8. Department of Biology, Indiana University, Bloomington, IN 47405

9. Department of Biology, Queen’s University, Kingston, ON K7L 3N6, Canada

10. Department of Plant Protection Biology, Swedish University of Agricultural Sciences, 234 22 Lomma, Sweden

11. School of Biological Sciences, Monash University, Melbourne 3800, Australia

12. Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, 753 26 Uppsala, Sweden

13. Norwegian Institute for Nature Research, Trondheim 7485, Norway

Abstract

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adaptation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic variation within populations (evolvability), as expected if genetic constraints are evolutionarily important. We further evaluate differences in divergence and evolvability–divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively with evolvability. Furthermore, trait divergence was greater for vegetative traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability–divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Funder

Vetenskapsrådet

Crafoordska Stiftelsen

Norges Forskningsråd

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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