The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

SUMMARY Pollination syndromes are a key component of flowering plant diversification, prompting questions about the architecture of single traits and genetic coordination among traits. Here, we investigate the genomic basis of extreme floral divergence between naturally hybridizing monkeyflowers Mimulus parishii (self-pollinated) and M. cardinalis (hummingbird-pollinated). We mapped quantitative trait loci (QTLs) for 18 (nine fully shared) pigment, pollinator reward and handling, dimensional, and flowering time traits in two F 2 hybrid growouts and recombinant inbred lines. We independently generated nearly isogenic lines (NILs) to dissect QTLs for two dimensional traits, pistil length and corolla size. Our multi-population approach revealed a highly polygenic basis (n = 190 QTLs total) for pollination syndrome divergence. For the set of nine fully shared traits, 39% (55/140) were unique to a single population, but we also identified several QTL hotspots within and across trait categories. The complementary NIL approach refined two pistil length QTLs but selected a corolla size QTL resistant to genetic dissection. Divergence between hummingbird- and self-pollinated sister species has a highly polygenic and largely uncoordinated genetic architecture. Our results extend understanding of speciation in a classic floral radiation and provide a robust framework for further molecular dissection and ecological genomics.