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Open Access Highly Accessed Research article

The role of genome and gene regulatory network canalization in the evolution of multi-trait polymorphisms and sympatric speciation

Kirsten HWJ ten Tusscher1 and Paulien Hogeweg2

Author Affiliations

1 Department of Scientific Computing, Simula Research Laboratory, P.O. Box 134,1325 Lysaker, Norway

2 Theoretical Biology and Bioinformatics Group, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands

BMC Evolutionary Biology 2009, 9:159  doi:10.1186/1471-2148-9-159

Published: 9 July 2009

Abstract

Background

Sexual reproduction has classically been considered as a barrier to the buildup of discrete phenotypic differentiation. This notion has been confirmed by models of sympatric speciation in which a fixed genetic architecture and a linear genotype phenotype mapping were assumed. In this paper we study the influence of a flexible genetic architecture and non-linear genotype phenotype map on differentiation under sexual reproduction.

We use an individual based model in which organisms have a genome containing genes and transcription factor binding sites. Mutations involve single genes or binding sites or stretches of genome. The genome codes for a regulatory network that determines the gene expression pattern and hence the phenotype of the organism, resulting in a non-linear genotype phenotype map. The organisms compete in a multi-niche environment, imposing selection for phenotypic differentiation.

Results

We find as a generic outcome the evolution of discrete clusters of organisms adapted to different niches, despite random mating. Organisms from different clusters are distinct on the genotypic, the network and the phenotypic level. However, the genome and network differences are constrained to a subset of the genome locations, a process we call genotypic canalization. We demonstrate how this canalization leads to an increased robustness to recombination and increasing hybrid fitness. Finally, in case of assortative mating, we explain how this canalization increases the effectiveness of assortativeness.

Conclusion

We conclude that in case of a flexible genetic architecture and a non-linear genotype phenotype mapping, sexual reproduction does not constrain phenotypic differentiation, but instead constrains the genotypic differences underlying it. We hypothesize that, as genotypic canalization enables differentiation despite random mating and increases the effectiveness of assortative mating, sympatric speciation is more likely than is commonly suggested.