4.4 Does homostyly spread among populations and why has it not
become fixed in Primula vulgaris?
Gene flow plays a central role in the spreading of mutations
(Morjan &
Rieseberg, 2004; Ralph & Coop, 2010), potentially contributing to the
migration of homostylous alleles among populations. In P.
vulgaris, previous hypotheses proposed that homostyly could have
migrated from initial places of origin to neighboring populations
through transport of pollen or seed, the former being more likely
(Crosby, 1949, 1960). Estimates of gene flow through pollen and seed in
this species indicated that dispersal is restricted to a maximum of a
few hundred meters from the parental plant (Cahalan & Gliddon, 1985),
but occasional pollen flow over 1–3 kilometers has also been reported
(Van Geert, Van
Rossum, & Triest, 2010). Our population genetic analyses support a
model of moderate levels of gene flow among populations (Nm =
1.96; Figure S3), while rejecting the hypothesis of a recent
fragmentation of an ancestral, widespread population. Accordingly, our
results do not support strong genetic differentiation among populations
(Figures 7A and B) or isolation by distance (Mantel test, P =
0.457), further favoring the hypothesis of gene flow among populations.
Moreover, the geographic distribution of CYPᵀ alleles in our
study indicates that 12 homostylous individuals from five populations
(D*11, T03, T04, T07 and T10) separated by 3-18 Km shared the sameCYPᵀ allele (CYPᵀ -2; Figure 4). This suggests that
homostylous alleles could have migrated between neighboring populations,
as the independent origin of exactly the same mutation should be
unlikely. Altogether, these results favor the conclusion that gene flow
might have facilitated the migration of homostylous alleles among
geographically close populations of P. vulgaris , confirming the
importance of gene flow for the spread of potentially advantageous
mutations.
A crucial question remains as to why homostyly has not become fixed inP. vulgaris despite automatic selfing advantage
(Fisher, 1941,
1949) and reproductive assurance
(Crosby, 1949). In
fact, the opposite has been found, since previous studies recorded the
loss or decrease of homostyles in revisited populations (Curtis &
Curtis 1985; Boyd et al., 1990). A possible explanation for the failure
of homostyly to completely replace heterostyly is that the negative
effects of inbreeding depression (Richards 1984; Goodwillie et al.,
2005) can outweigh the advantages of homostyly (Piper et al., 1984; Boyd
et al., 1990). Two recent studies investigated the relationship between
inbreeding depression and the spread of self-compatibility, finding
contrasting results. In experimental populations of Linaria
cavanillesi , self-compatible individuals with no inbreeding depression
displaced self-incompatible individuals in just three generations
(Voillemot & Pannell, 2017; Voillemot, Encinas-Viso, & Pannell,
2019). In
contrast, inbreeding depression values of 0.54 prevented the spread of
SC plants within experimental patches of SI plants inLaevenworthia alabamica (Layman, Fernando, Herlihy, & Busch,
2017) . Our
estimate of inbreeding depression (0.58) in P. vulgaris is closer
to the latter study, suggesting that inbreeding depression might be
sufficiently high to prevent the fixation of homostyly within
populations. While theory proposes that increased selfing should purge
inbreeding depression over time by eliminating recessive deleterious
alleles from populations (Schemske & Lande,
1985),
transitions to homostyly in P. vulgaris may be too recent for the
purging process to have occurred. Moreover, recessive deleterious
alleles could have been re-introduced into populations via gene
flow, thus slowing the decrease of inbreeding depression. Our study
estimated moderate levels of gene flow among populations of P.
vulgaris (Nm = 1.96; Supplementary Figure S3), implying that
re-introduction of genetic load is feasible. Overall, our findings
suggest that inbreeding depression plays a key role in maintaining
heterostylous morphs within populations despite the reproductive
advantages of homostyly.