Recovery from hybrid breakdown reveals a complex genetic architecture of
mitonuclear incompatibilities
Abstract
Reproductive isolation is often achieved when genes that are neutral or
beneficial in their genomic background become functionally incompatible
in a foreign genome, causing inviability, sterility or low fitness in
hybrids. Recent studies suggest that mitonuclear interactions are among
the initial incompatibilities to evolve at early stages of population
divergence across taxa. Yet, it is unclear whether mitonuclear
incompatibilities involve few or many regions in the nuclear genome. We
employ an experimental evolution approach starting with unfit F2
interpopulation hybrids of the copepod Tigriopus californicus, in which
compatible and incompatible nuclear alleles compete in a fixed
mitochondrial background. After about nine generations, we observe a
generalized increase in population size and in survivorship, suggesting
efficiency of selection against maladaptive phenotypes. Whole genome
sequencing of evolved populations showed some consistent allele
frequency changes across the three replicates of each reciprocal cross,
but markedly different patterns between mitochondrial background. In
only a few regions (~6.5% of the genome), the same
parental allele was overrepresented irrespective of the mitochondrial
background. About 33% of the genome shows allele frequency changes
consistent with divergent selection, with the location of these genomic
regions strongly differing between mitochondrial backgrounds. The
dominant allele matches the mitochondrial background in 87 and 89% of
these genomic regions, consistent with mitonuclear coadaptation. These
results suggest that mitonuclear incompatibilities have a complex
polygenic architecture that differs between populations, potentially
generating genome wide barriers to gene flow between closely related
taxa.