Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals

Philosophical Transactions of the Royal Society B Biological Sciences, vol. 377, pp. 20210199

Abstract

Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

Authors 6

1. Emma L. Berdan corresponding Aachen Institute of Biology Leiden Naturalis Biodiversity Center

   Leiden University · Naturalis Biodiversity Center · University of Gothenburg

   Affiliation as printed

   Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 RA, Leiden, The Netherlands

   Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, The Netherlands

   Tjarnö Marine Laboratory, Department of Marine Sciences, University of Gothenburg, 45296 Stromstad, Sweden

2. Alexandre Blanckaert

   University of Wisconsin–Madison · University of Lisbon

   Affiliation as printed

   Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI, USA

   cE3c – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016, Lisboa, Portugal

3. Roger Kenneth Butlin

   University of Gothenburg · University of Sheffield

   Affiliation as printed

   Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK

   Tjarnö Marine Laboratory, Department of Marine Sciences, University of Gothenburg, 45296 Stromstad, Sweden

4. Thomas Flatt

   University of Fribourg

   Affiliation as printed

   Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland

5. Tanja Slotte

   Stockholm University · Science for Life Laboratory

   Affiliation as printed

   Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, 106 91 Stockholm, Sweden

6. Ben Wielstra Aachen Institute of Biology Leiden Naturalis Biodiversity Center

   Leiden University · Naturalis Biodiversity Center

   Affiliation as printed

   Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 RA, Leiden, The Netherlands

   Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, The Netherlands