Indirect Evolution of Hybrid Lethality Due to Linkage with Selected Locus in Mimulus guttatus

Abstract

Ecological selection on an adaptive allele causes a tightly linked hybrid incompatibility factor to rapidly hitchhike to high frequency in a population of the wildflower Mimulus guttatus.

Abstract

Most species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductive timing, courtship behavior, or pollinator attraction may prevent interbreeding in nature, causing reproductive isolation. But does ecological adaptation cause reproductive incompatibilities such as hybrid sterility or lethality? Although several genes causing hybrid incompatibilities have been identified, there is intense debate over whether the genes that contribute to ecological adaptations also cause hybrid incompatibilities. Thirty years ago, a genetic study of local adaptation to copper mine soils in the wildflower Mimulus guttatus identified a locus that appeared to cause copper tolerance and hybrid lethality in crosses to other populations. But do copper tolerance and hybrid lethality have the same molecular genetic basis? Here we show, using high-resolution genome mapping, that copper tolerance and hybrid lethality are not caused by the same gene but are in fact separately controlled by two tightly linked loci. We further show that selection on the copper tolerance locus indirectly caused the hybrid incompatibility allele to go to high frequency in the copper mine population because of hitchhiking. Our results provide a new twist on Darwin's original supposition that hybrid incompatibilities evolve as an incidental by-product of ordinary adaptation to the environment.

Author Summary

Adaptive evolution by natural selection is the primary force generating biological diversity. A critical question is whether the evolution of hybrid incompatibility, which is essential for the maintenance of species diversity, is caused by adaptive evolution. In this article, we investigate one of the most widely cited examples of ecological divergence driving the evolution of reproductive incompatibility, the strong association between hybrid lethality and copper tolerance in a copper mine population of the wildflower Mimulus guttatus. Hybrid lethality and tolerance of high levels of copper co-segregate as a single Mendelian locus. While copper tolerance and hybrid lethality are nearly universal in the mine population at Copperopolis, California, they are absent from adjacent off-mine populations, suggesting that reproductive isolation evolved rapidly as a pleiotropic by-product of recent adaptation to the mine environment. We find that copper tolerance and hybrid lethality are controlled by distinct loci, in tight genetic linkage. We also demonstrate that this genomic region has experienced strong recent selection and conclude that ecological selection for copper tolerance indirectly caused the neighboring hybrid lethality allele to hitchhike to high frequency. To our knowledge, this is the first case to demonstrate that reproductive isolation factors can evolve as an incidental by-product of adaptation to novel environments through genetic hitchhiking.