Phylogenomic patterns of divergence and gene flow detail the evolution of reinforcement and hybrid speciation inPhloxwildflowers

Abstract

It is becoming increasingly clear that the evolutionary histories of many groups of organisms are riddled with reticulation. Some clades of organisms appear to be hotspots of speciation by hybridization and gene flow. For example, there are two cases of reinforcement and up to nine cases of hypothesized hybrid speciation in the eastern standing Phlox (Polemoniaceae) wildflowers. However, the relationships of these taxa and the hypotheses about their evolution have received limited attention with genomic data. We performed a comprehensive phylogenomic study of the eastern standing Phlox to resolve their evolutionary relationships and test long-standing hypotheses about if and how hybridization and gene flow acted as creative forces in their diversification. Our phylogenomic analyses on genome-wide markers provides resolution into the evolutionary relationships of thirty-two eastern standing Phlox taxa, including well-supported non-monophyletic relationships across species complexes. Explicit tests for introgression support gene flow occurring alongside the evolution of one of the two cases of reinforcement, and patterns of divergence and gene flow support one of the five hypothesized homoploid hybrid speciation events. Additionally, comparative read mapping allowed assignment of putative subgenome ancestries for four allotetraploids hybrid species. Our findings demonstrate the utility and importance of phylogenomics in confirming hypothesized evolutionary histories of non-model systems and add to the growing evidence that gene flow across species boundaries can play a role in the generation of novel biodiversity.

Noteworthy Collections: First Record of a Natural Hybrid Between Phlox divaricata ssp. laphamii (Alph. Wood) Wherry and Phlox pilosa ssp. sangamonensis (Levin & D.M. Sm.)

“…pilosa L. populations are a monophyletic clade that is distinct from northern P. pilosa ssp. pilosa populations (Garner et al 2022, preprint). In the Garner et al (2022 preprint) study, P. pilosa ssp.…”

“…pilosa populations (Garner et al 2022, preprint). In the Garner et al (2022 preprint) study, P. pilosa ssp. sangamonensis was closely related to P. pilosa ssp.…”

Mismatch between pollen and pistil size causes asymmetric mechanical reproductive isolation acrossPhloxspecies

“…Because the variation in style length across species is not associated with other major transitions in reproductive strategy, it is challenging to infer what drove the evolution of style length variation in this system. Across the phylogeny of Phlox most species have long-styles, and the monophyletic clade of short-styled species is nested within the broader group of long-styled species (Garner et al ., 2024). This phylogenetic pattern suggests that the ancestor of the short-styled Phlox had a long style, and that short-style/small pollen is a derived state having evolved just once.…”

Acis-regulatory point mutation at a R2R3-Myb transcription factor contributes to speciation by reinforcement inPhlox drummondii

“…To determine the direction of evolution of the associated alleles at SNP1 and SNP2 we compared the sequences of the PdMyb1 proximal promoter in dark sympatric and light allopatric P. drummondii individuals to representatives of the other annual Phlox species, P. roemeriana and P. cuspidata, and a perennial outgroup species, P. pilosa ssp. pilosa (Garner et al, 2022). Aside from the dark flowers observed in sympatric populations of P. drummondii, all four species display a light flower color.…”