Patterns of hybrid seed inviability in perennials of theMimulus guttatussp. complex reveal a potential role of parental conflict in reproductive isolation

Abstract

SummaryGenomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here we describe M. decorus; a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus conform to the predictions of parental conflict: (1) reciprocal F1s exhibit size differences and parent-of-origin specific endosperm defects, (2) the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI, and (3) inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, while all populations are largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than mating system may also influence the rate of parental conflict driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation.

Parallel patterns of development between independent cases of hybrid seed inviability in Mimulus

“…All lines of M. decorus show consistent patterns of strong, and asymmetric hybrid seed inviability when crossed with M. guttatus , but the two genetic clades showed oppositely asymmetric HSI (Figure 1; Odell Creek: X 2 = 4598, df =3, p<0.0001; IMP: X 2 = 2969, df =3, p<0.0001). Northern M. decorus produces entirely inviable seeds when the maternal donor in these crosses, while southern M. decorus produces entirely inviable seeds when the paternal donor (and some inviable seeds when the maternal donor; Figure 1; Coughlan et al . 2018).…”

“…Previous works suggests that morphologically assessed viability is a good proxy for germination proclivity (Garner et al . 2016; Coughlan et al . 2018).…”

“…We previously reported a wide diversity of hybrid seed barriers between M. guttatus and its morphological variant, M. decorus which confer strong reproductive isolation (Coughlan et al . 2018).…”

“…2018). We found that M. decorus is multiple biological species; a diploid northern clade that exhibits strong asymmetric HSI when it is the maternal donor in crosses to M. guttatus ; a diploid southern clade that exhibits strong asymmetric HSI when it is the paternal donor in crosses to M. guttatus; and at least one tetraploid taxon that exhibits variable levels of HSI (Coughlan et al . 2018).…”

“…2018). Because the direction of inviability differs between M. guttatus and each clade of diploid M. decorus , there must be independent evolution of maternal and paternal alleles causing inviability between northern and southern M. decorus , even though they are each other’s closest relative (Coughlan et al . 2018).…”