Inversion arose in the common ancestor not after hybridization?

Diler led the interesting discussion on March 25th about Fuller et al. (2018) study demonstrating the inversion that is important in speciation between Drosophila persimilis (abbreaviated as per) and D. pseudobscura(abbreaviated as pse) existed due to incomplete lineage sorting of ancestral polymorphism. This study led to the intriguing possibility that the structural variations do not have to be a consequence of divergent selection or reinforcement wiring barrier loci together (Hartl 1977), but could be segregating as the speciation progressed, potentially fuelling future speciation events (see figure below).

There is sex chromosome polymorphism within per: the right arm of X chromosome is inverted (ST) compared to pse, while the sex-ratio chromosome (SR) version is collinear with pse. Fuller et al. (2018) investigated whether the collinearity between pse and per XR is due to a secondary inversion of ST background; or a single chromosomal arrangement existed in the common ancestral population. With window-based relative node depth (RND) statistics, normalized dxy relative to divergence to the outgroup (to adjust for difference of mutation rate among genetic regions), Fuller et al. (2018) showed that within the inversion, per inversion polymorphisms demonstrated greater RND relative to pse ST, than the RND between inversion polymorphisms within per. The RND within the collinear regions were drastically reduced. Such pattern was thought as support for incomplete lineage sorting of the per inversion polymorphisms.

However, if the per ST and SR polymorphism existed for a long time (in the ancestral population of per and pse, see figure below), shouldn’t per ST and SR demonstrate comparable RND to the RND between pse ST and any variant of per inversions? The maximum likelihood model section was a nice attempt, however since no AIC value was shown, we can not rule out that the isolation-with initial migration model fits the data better because there are more parameters in it. At the end, this paper provides a beautiful idea that we are not fully convinced about.

Reference

Fuller, Z. L., C. J. Leonard, R. E. Young, S. W. Schaeffer, and N. Phadnis. 2018. Ancestral polymorphisms explain the role of chromosomal inversions in speciation. PLoS Genet. 14:e1007526.

Hartl, D. L. 1977. How does the Genome Congeal? Pp. 65–82 in Measuring Selection in Natural Populations.