Divergent selection and climate adaptation fuel genomic differentiation between sister species of Sphagnum (peat moss)

Abstract

Background and aims: New plant species can evolve through the reinforcement of reproductive isolation via local adaptation along habitat gradients. Peat mosses (Sphagnaceae) are an emerging model system for the study of evolutionary genomics and have well-documented niche differentiation among species. Recent molecular studies have demonstrated that the globally distributed species Sphagnum magellanicum is a complex of morphologically cryptic lineages that are phylogenetically and ecologically distinct. Here, we describe the architecture of genomic differentiation between two sister species in this complex known from eastern North America: the northern S. diabolicum and the largely southern S. magniae.

Methods: We sampled plant populations from across a latitudinal gradient in eastern North America and performed whole genome and restriction-site associated DNA sequencing. These sequencing data were then analyzed computationally.

Key results: Using sliding-window population genetic analyses we find that differentiation is concentrated within 'islands' of the genome spanning up to 400 kb that are characterized by elevated genetic divergence, suppressed recombination, reduced nucleotide diversity and increased rates of non-synonymous substitution. Sequence variants that are significantly associated with genetic structure and bioclimatic variables occur within genes that have functional enrichment for biological processes including abiotic stress response, photoperiodism and hormone-mediated signalling. Demographic modelling demonstrates that these two species diverged no more than 225 000 generations ago with secondary contact occurring where their ranges overlap.

Conclusions: We suggest that this heterogeneity of genomic differentiation is a result of linked selection and reflects the role of local adaptation to contrasting climatic zones in driving speciation. This research provides insight into the process of speciation in a group of ecologically important plants and strengthens our predictive understanding of how plant populations will respond as Earth's climate rapidly changes.

Keywords: Sphagnum; climate; comparative genomics; molecular adaptation; selection; speciation.

Fig. 1.

Populations from two sister species in the Sphagnum magellanicum complex were sampled from along a latitudinal gradient in eastern North America. (A) DNA sequences from plants of S. diabolicum (orange) and S. magniae (blue) were obtained using full genome resequencing (circles) and RADseq (squares). (B) A hardwood hammock in Florida representing the typical habitat of the largely southern species, S. magniae. (C) A kettlehole bog in New York representing the typical habitat of the northern species, S. diabolicum.

Fig. 2.

Molecular data demonstrate genetic differentiation between S. diabolicum (orange) and S. magniae (blue). (A) Ancestry estimation using ADMIXTURE suggests that most samples are of non-admixed ancestry but some show evidence of admixture where the species’ ranges overlap. (B) Principal component analyses demonstrate that the two species are genetically distinct. (C) Coalescent analyses favour a model of secondary contact with gene flow initially restricted following divergence from a common ancestor (grey) but occurring more recently. Rectangle width reflects the log₁₀-transformed estimates of effective population size.

Fig. 3.

The genomic landscape of differentiation between sister species of Sphagnum is heterogeneous and shows hallmarks of linked selection. (A) Manhattan plot of F_ST estimated across 10-kb sliding windows. Mean F_ST across the genome is shown by a solid blue line and the threshold for F_ST outliers is depicted by a dotted blue line. (B) F_ST is negatively correlated with reduced nucleotide diversity (π) but not genetic distance (D_xy) across all autosomal sliding windows. (C) There are ‘islands’ of genomic differentiation within chromosomes, such as chromosome 16 shown here, that have high levels of genetic divergence (F_ST and D_xy) and low nucleotide diversity.

Fig. 4.

Integration of results across analyses highlights the genetic loci responsible for local adaptation. (A) Venn diagram showing single nucleotide polymorphisms (SNPs) that are fixed differences between species, significantly associated with genetic structure as inferred using pcadapt, and significantly associated with bioclimatic variables using redundancy analysis (RDA) and latent factor mixed model (LFMM) analysis. (B) Upset plot showing the genes that have fixed missense differences between species, are present in genomic islands of differentiation (F_ST outliers) and lie within 5 kb of SNPs significantly associated with genetic structure or bioclimatic variables.