Gene Duplication in Mimulus Underlies Parallel Floral Evolution via Independent trans-Regulatory Changes

Identifying the genetic basis of parallelism reveals the means by which evolution repeats itself and shows what aspects-if any-may be predictable [1]. The recently tetraploid luteus group of Mimulus [2] contains five species native to central Chile [3], three of which have evolved extensive red floral pigmentation using at least two distinct loci [4]. Here we show that the parallel evolution of petal lobe anthocyanin (PLA) pigmentation in M. cupreus and M. luteus var. variegatus occurred via separate yet strikingly similar mechanisms. In each case, a dominant, single-locus gain of pigmentation [4] maps to a genomic region (pla1 and pla2, respectively) containing adjacent, apparently recently duplicated paralogs of MYB anthocyanin-regulating transcription factors. Interestingly, candidate genes in pla1 and pla2 are themselves related by an older duplication. In both cases, pla genotype cosegregates with expression of multiple genes in the anthocyanin biosynthetic pathway, revealing a mechanism of coordinated trans-regulatory expression changes across functionally related enzyme-encoding genes. We conclude that in this instance, evolution has repeated itself with marked consistency. Duplication has enabled that repetition to occur using two physically independent but functionally similar loci, highlighting the importance of genomic complexity to the evolutionary process.