Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation

Adaptation to contrasting environments occurs when advantageous alleles
accumulate in each population, but it remains largely unknown whether
these same advantageous alleles create genetic incompatibilities that can
cause intrinsic reproductive isolation leading to speciation. Identifying
alleles that underlie both adaptation and reproductive isolation is
further complicated by factors such as dominance and genetic interactions
among loci, which can affect both processes differently and obscure
potential links between adaptation and speciation. Here, we use a
combination of field and glasshouse experiments to explore the connection
between adaptation and speciation while accounting for dominance and
genetic interactions. We created a hybrid population with equal
contributions from four contrasting ecotypes of Senecio lautus
(Asteraceae), which produced hybrid genomes both before (F1 hybrid
generation) and after (F4 hybrid generation) recombination among the
parental ecotypes. In the glasshouse, plants in the second generation (F2
hybrid generation) showed reduced fitness as a loss of fertility, but
fertility was recovered in subsequent generations suggesting that genetic
variation underlying fertility reduction was lost in subsequent
generations. To quantify the effects of losing genetic variation at the F2
generation on the fitness of later generation hybrids, we used a
reciprocal transplant to test for fitness differences between parental
ecotypes, and F1 and F4 hybrids in all four parental habitats. Compared to
the parental ecotypes and F1 hybrids, variance in F4 hybrid fitness was
lower, and lowest in habitats that showed stronger native-ecotype
advantage, suggesting that stronger natural selection for the native
ecotype reduced fitness variation in the F4 hybrids. Fitness trade-offs
that were present in the parental ecotypes and F1 hybrids were absent in
the F4 hybrid. Together, these results suggest that the genetic variation
lost after the F2 generation was likely associated with both adaptation
and intrinsic reproductive isolation among populations adapted to
contrasting environments.