Increased productivity in hybrid lines suggests recovery
from fitness breakdown
Previous long-term evolution experiments in T. californicus have
found varying degrees of fitness recovery from F2 breakdown (Hwanget al. 2011; Pritchard et al. 2012; Hwang et al.2016), presumably because hybrids with matching mitonuclear complexes
would have higher generalized fitness than their siblings with unmatched
mitonuclear complexes. Thus, matched (coadapted) nuclear alleles would
outcompete unmatched (incompatible) alleles over multiple generations
(Fig. 1). However, those experimental lines started with a mix of pure
parental individuals, so that unmixed nuclear genotypes and the two
mitochondria could persist well into the experiment. This design made it
challenging to distinguish between fitness recovery caused by the
exclusion of incompatible nuclear alleles in a hybrid background, from
fitness recovery caused by competition and drift of pure parental
genotypes. In contrast, we initiated experimental lines with F2 hybrids
and in fixed mitochondrial backgrounds, so that differences in fitness
and allele frequency can only be explained by competition between
parental nuclear alleles.
Our results show that control parental populations went extinct within
two months of experimental evolution, probably due to inbreeding
depression described in this species (Palmer & Edmands 2000). In
contrast, almost all hybrid lines survived the nine months of
experimental evolution, with most showing an increase in population size
(from 1.1 to 9-fold; Fig. 2A). From the many traits known to be involved
in hybrid breakdown in T. californicus (Burton 1990a; b; Edmands
1999; Edmands & Burton 1999; Ellison & Burton 2006; 2008a; 2010), we
have assessed recovery in two: female fecundity and nauplii
survivorship. In respect to fecundity, we observed a strong F2 breakdown
(P-values< 0.017), and no recovery in evolved hybrid lines,
irrespective of the mitochondrial background (Fig. 2B). This suggests
that this is a complex trait that could not evolve in these experimental
conditions of population size, number of generations and selective
regime.
In contrast, with respect to survivorship, we observed less severe
breakdown in F2 generation (P-values> 0.125). Notably,
survivorship breakdown was stronger in the F2 hybrids with the SC
mitochondria, suggesting that selection imposed by mitonuclear
incompatibilities is stronger in SC relative to SD mitochondrial
background. In both backgrounds, several hybrid lines recovered up to or
beyond parental fitness levels (P-values< 0.043; Fig. 2C),
suggesting that recombination and selection over nine months were
sufficient to cause evolution at this trait. Rescue in survivorship up
to or beyond parental fitness levels has also been reported in F9
recombinant hybrid lines of T. californicus (Pereira et
al. 2014), suggesting that the genetic architecture of this specific
trait might be relatively simple. Nevertheless, we note that the line
showing the largest increase in productivity (9-fold increase in SD6),
did not show recovery in survivorship, therefore selection imposed by
our experimental design is likely multifarious and responding with
phenotypes beyond those measured here. Future studies employing directed
selection on a specific trait (Healy & Burton 2020) over many
generations of experimental evolution may provide insights into this
question.