Abstract
Author SummaryAdaptive 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.
Highlights
Adaptation to local environmental conditions by natural selection is the primary cause of evolutionary change in natural populations
Genetic Mapping To determine whether copper tolerance and hybrid lethality are controlled by the same locus, we conducted a high-resolution genetic mapping experiment
In order to genetically map these phenotypes with high resolution, we used a near isogenic line (NIL) created through recurrent backcrossing of a Copperopolis by Cerig35 F1 to lines derived from Stinson Beach, California
Summary
Adaptation to local environmental conditions by natural selection is the primary cause of evolutionary change in natural populations. Classic models of the evolution of hybrid incompatibility, independently developed by Bateson [5], Dobzhansky [6], and Muller [7] (BDM), predict that alleles at different loci may accumulate within distinct lineages, and they may be neutral or adaptive in an ancestral population, they will produce deleterious interactions when brought together by hybridization. This model is thoroughly supported by genetic mapping studies of hybrid incompatibility loci. The role of natural selection in driving the evolution of incompatibility alleles continues to be an area of rich investigation [8,9,10]
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