Parental population range expansion before secondary contact promotes heterosis

Population genomic analysis of hybrid zones is instrumental to our
understanding of the evolution of reproductive isolation. Many
temperate hybrid zones are formed by the secondary contact between two
parental populations that have undergone post-glacial range expansion.
Here we show that explicitly accounting for historical parental isolation
followed by range expansion prior to secondary contact is fundamental for
explaining genetic and fitness patterns in these hybrid zones.
Specifically, ancestral population expansion can result in allele surfing
where neutral or slightly deleterious mutations drift to high frequency at
the expansion front. If these surfed deleterious alleles are recessive,
they can contribute to substantial heterosis in hybrids produced at
secondary contact, counteracting negative effects of
Bateson-Dobzhansky-Muller incompatibilities (BDMIs) hence weakening
reproductive isolation. When BDMIs are linked to such recessive
deleterious alleles the fitness benefit of introgression at these loci can
facilitate introgression at the BDMIs. The extent to which this occurs
depends on the strength of selection against the linked deleterious
alleles and the distribution of recombination across the chromosome.
Finally, surfing of neutral loci can alter the expected pattern of
population ancestry, thus accounting for historical population expansion
is necessary to develop accurate null genomic models of secondary-contact
hybrid zones.