Premise: Hybridization is an important evolutionary process across all groups of embryophyte land plants, but relatively little is known about hybridization and introgression in spore producing plants with a dominant gametophyte life cycle stage (i.e., bryophytes). The Sphagnum magellanicum complex, with four North American species, is proving to be a valuable system for studying population genomics, speciation, and climate adaptation. This paper focuses on hybridization between the four species, with focus on a regional zone where virtually all plants in the two most recently diverged species (S. diabolicum, S. magniae) show genetic admixture.

Methods: Analyses of population genetics and introgression utilized three types of molecular data: RADseq, “RADseq-like” data derived from in silico digestion of genome sequences, and species-specific barcode markers developed previously for this group. 582 gametophytes were sampled from 79 collecting sites representing 23 U.S. states and five Canadian provinces, from 27 ^o to 56^o N. A range of analytical methods were employed: phylogeny reconstruction, STRUCTURE to assess individual genetic admixture, demographic modeling to estimate the timing and extent of interspecific gene flow, and comparative genomics to evaluate the occurrence and locations of introgressed SNPs.

Results: Low but significant gene flow was detected among all pairwise combinations of extant species as well as between ancestral lineages and those species. Greater genetic similarities among species where they occur sympatrically within peatlands suggests that hybridization is on-going. Hybridization between S. diabolicum and S. magniae is especially pronounced and plants in a regional zone from North Carolina to New Jersey are genetically admixed. Demographic analyses all indicate that this admixture reflects hybridization, not just incomplete lineage sorting. Introgressed SNPs were detected across all chromosomes but introgressed SNPs fixed in genetically pure samples of the two species were concentrated on four autosomes: 2, 7, 14, and 19. Introgression block sizes and numbers were positively correlated with the level of genetic admixture. Patterns of genomic admixture/introgression were significantly correlated with climate variation across collection sites within the hybrid zone.

Conclusions: Previous analyses indicated that climate adaptation has played an important role in speciation within this group, especially the divergence of warm-temperate to subtropical S. magniae from cold-temperate to boreal S. diabolicum. This work shows that the genomic structure of plants in a regional hybrid zone between S. magniae and S. diabolicum is also structured by climate adaptation and strengthens the value of this group for learning more about both speciation and climate adaptation.