Introgression, Population Structure, and Systematics of the Sphagnum capillifolium complex

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2023

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Abstract

How geographical distance and historical events affect patterns of population divergence and gene flow is an important question in evolution and biogeography. Sphagnum subgenus Acutifolia is one of the four major subgenera of Sphagnum peatmoss comprising numerous species with broad geographic ranges and diverse ecological niches within wetland habitats. One group of particular interest within the subgenus is the S. capillifolium complex which contains at least seven closely related species. Five species within the complex are circumboreal and all have overlapping geographic ranges, one species is endemic to subtropical region of eastern North America, and one species is in the tropical regions of Central and South America. The presence of both species with overlapping and disjunct distributions makes the Sphagnum capillifolium complex a natural experiment to investigate gene flow and population divergence in multiple phylogenetic scales (within and between species). Chapter 1 describes patterns of phylogenetic discordance across the genome in the Sphagnum capillifolium complex using whole genome resequencing data. The species tree phylogeny was generally well supported but phylogenetic discordance among genomic regions was prevalent, especially at nodes in the backbone. Alternative topologies for each of the backbone nodes were not random, suggesting the presence of introgression, in addition to incomplete lineage sorting (ILS). Analyses of introgression signals using ABBA/BABA tests and branch length distributions (QuIBL) showed that there were several possible introgression events within the S. capillifolium complex involving both extant and ancestral species. Most of the introgression events occurred between species that currently have overlapping geographic ranges. Further investigation of one introgression event using comparisons of terminal branch lengths showed that the biased pattern of shared derived alleles likely derives from introgression, not ancient polymorphism. These findings show that introgression played a significant role in generating phylogenetic incongruence within the S. capillifolium complex. We also show that the use of multiple phylogenomic methods and investigating localized genomic regions are essential to infer complex introgression scenarios. Chapter 2 describes phylogenetic structure of Sphagnum subgenus Acutifolia and population structure of circumboreal species within the S. capillifolium complex. Genome scale data (RAD-seq) was generated for the subgenus, with an intensive population sampling of circumboreal species within the S. capillifolium complex. Most of the species are resolved as monophyletic, although relationships among species are weakly supported in some parts of the phylogeny. Some currently recognized species are phylogenetically discernable while others are not distinguishable from the well-supported species. Within the S. capillifolium complex, five circumboreal species show similar patterns of population structure. One population system comprises plants in eastern North America and Europe, and sometimes includes plants from eastern Eurasia and the Pacific Northwest of North America. Another group comprises plants in the Pacific Northwest, or around the Beringian and Arctic regions. Our results suggest that populations of circumboreal species survived in multiple refugia during the last glacial maximum (LGM). Long-distance dispersal out of refugia, population bottlenecks, and possible adaptations to conditions unique to each refugium contribute to current geographic patterns. There are patterns of genetic admixture among distinct genotype groups within species in some restricted areas. Alaska is a hotspot for both intraspecific genetic diversity and admixture. These genetic results indicate the important role of historical events, especially Pleistocene glaciation, in shaping the complex population structure of plants with broad distribution ranges. Chapter 3 assesses the pattern of gene flow between a pair of sister Sphagnum species within the S. capillifolium complex: S. warnstorfii and S. talbotianum. The two species have different distribution ranges: S. warnstorfii is circumboreal while S. talbotianum is circumarctic, but they overlap in Alaska. Genetic data from chapter 2 were used in this chapter. Analyses of interspecific gene flow and population sizes were accomplished using coalescent simulations of site frequency spectra (SFSs), and the signature of gene flow was further corroborated by ABBA/BABA statistics. Our results indicate that S. warnstorfii and S. talbotianum were isolated after divergence. S. warnstorfii was relatively recently established in Alaska and Alaska is the only region that shows evidence of gene flow between S. talbotianum and S. warnstorfii. Gene flow occurred in only one direction from S. talbotianum into S. warnstorfii, which can possibly help S. warnstorfii survive in subarctic conditions. Molecular evidence further suggests gene flow from Alaska S. warnstorfii to other regional populations of that species. S. warnstorfii suffered a stronger population bottleneck than S. talbotianum, suggesting that Beringia could have harbored larger populations during the last glacial maximum than other, likely more southern, refugia. Although the two species are very closely related, S. talbotianum has larger pores on the convex surfaces of branch leaf apices than S. warnstorfii. Our results represent a case study of a recent gene flow between geographically sympatric peatmoss species using genomic data. Our results also support S. talbotianum as a distinct species from S. warnstorfii.

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Imwattana, Karn (2023). Introgression, Population Structure, and Systematics of the Sphagnum capillifolium complex. Dissertation, Duke University. Retrieved from https://hdl.handle.net/10161/29122.

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