Supergenes and their role in evolution

Abstract

Adaptation is commonly a multidimensional problem, with changes in multiple traits required to match a complex environment. This is epitomized by balanced polymorphisms in which multiple phenotypes co-exist and are maintained in a population by a balance of selective forces. Consideration of such polymorphisms led to the concept of the supergene, where alternative phenotypes in a balanced polymorphism segregate as if controlled by a single genetic locus, resulting from tight genetic linkage between multiple functional loci. Recently, the molecular basis for several supergenes has been resolved. Thus, major chromosomal inversions have been shown to be associated with polymorphisms in butterflies, ants and birds, offering a mechanism for localised reduction in recombination. In several examples of plant self-incompatibility, the functional role of multiple elements within the supergene architecture has been demonstrated, conclusively showing that balanced polymorphism can be maintained at multiple coadapted and tightly linked elements. Despite recent criticism, we argue that the supergene concept remains relevant and is more testable than ever with modern molecular methods.

Figure 1

Convergent evolution of SI mechanisms across flowering plants. The S-RNases are shared between Asterid and Rosid lineages, which diverged c. 100 mya. Genera where SI has been documented are annotated within each family. Phylogenetic relationships sourced from http://tolweb.org, divergence estimate from http://timetree.org.

Figure 2

(a) Different forms of the butterfly H. numata are associated with different genome arrangements in the region of the P supergene. Forms of H. numata are shown above the horizontal line, with their corresponding models beneath. Photos from Mathieu Joron. (b) Representation of the rearrangements on chromosome 2 of Zonotrichia albicollis associated with reproductive dimorphism. The inversions cover c. 105 Mb. Population genetics figures from Thomas et al. (2008). Figures for collinear region are for the marker SUPT3H. Pi values for the inverted region are for both loci considered together, and each separately. Photographs modified from Figure 1 of Horton et al. (2012).