Genotype, phenotype and linkage data for Mimulus parishii x M. cardinalis hybrid incompatibility study

The evolution of genomic incompatibilities causing postzygotic barriers to
hybridization is a key step in species divergence. Incompatibilities take
two general forms – structural divergence between chromosomes leading to
severe hybrid sterility in F1 hybrids and epistatic interactions between
genes causing reduced fitness of hybrid gametes or zygotes
(Dobzhansky-Muller incompatibilities). Despite substantial recent progress
in understanding the molecular mechanisms and evolutionary origins of both
types of incompatibility, how each behaves across multiple generations of
hybridization remains relatively unexplored. Here, we use genetic mapping
in F2 and RIL hybrid populations between the phenotypically divergent but
naturally hybridizing monkeyflowers Mimulus cardinalis and M. parishii to
characterize the genetic basis of hybrid incompatibility and examine its
changing effects over multiple generations of experimental hybridization.
In F2s, we found severe hybrid pollen inviability (< 50% reduction
vs. parental genotypes) and pseudolinkage caused by a reciprocal
translocation between Chromosomes 6 and 7 in the parental species. RILs
retained excess heterozygosity around the translocation breakpoints, which
caused substantial pollen inviability when interstitial crossovers had not
created compatible heterokaryotypic configurations. Strong transmission
ratio distortion and inter-chromosomal linkage disequilibrium in both F2s
and RILs identified a novel two-locus genic incompatibility causing
sex-independent gametophytic (haploid) lethality. The latter interaction
eliminated three of the expected nine F2 genotypic classes via F1 gamete
loss without detectable effects on the pollen number or viability
of F2 double heterozygotes. Along with the mapping of numerous
milder incompatibilities, these key findings illuminate the complex
genetics of plant hybrid breakdown and are an important step toward
understanding the genomic consequences of natural hybridization in this
model system.