Evolutionary history of theAsplenium scolopendriumcomplex (Aspleniaceae), a relictual fern with a northern pan-temperate disjunct distribution

Abstract

Asplenium scolopendrium is distributed in northern temperate forests with many global biogeographic disjunctions. The species complex of A. scolopendrium has been generated by spatial segregation coupled with divergent evolution. We elucidated the biogeographic history of the A. scolopendrium complex by exploring its origin, dispersal and evolution, thus providing insights into the evolutionary history of the Tertiary floras with northern pan-temperate disjunct distributions. The results revealed that all infraspecific taxa descended from a widely distributed common ancestor in the Northern Hemisphere. This pan-temperate ancestral population formed by unidirectional westward dispersal from European origins primarily during the Early Eocene when the Earth’s climate was much warmer than today. The splitting of European, American and East Asian lineages occurred during the Early Miocene due to geo-climatic vicariances. Polyploidy events in the American ancestral populations created additional reproductive barriers. The star-shaped haplotypes in each continent indicated that local disjunctions also led to derived genotypes with potential to diverge into different taxa. This intracontinental lineage splitting is likely related to latitudinal range shift and habitat fragmentation caused by glacial cycles and climate change during the Pleistocene. The evolutionary history of the A. scolopendrium complex supported the Boreotropical hypothesis exhibiting range expansion during the Early Eocene Climatic Optimum.

Molecular phylogenetic assessment of three major taxa in the Asplenium scolopendrium complex (Aspleniaceae)

“…-Overall, there was congruence between phylogenetic trees/networks based on maternally (plastid DNA) and biparentally inherited (nuclear DNA) sequences for the three major taxa of the Asplenium scolopendrium complex, illustrating that reticulation among these three taxa did not likely occur. Despite potentials of long-distance dispersal in ferns, the three major taxa of A. scolopendrium appeared to have complete lineage sorting due to a high degree of geographic separation and a long history of lineage divergences, likely beginning from the Late Pliocene (Heo & al., 2022). Thus, the existing taxonomic treatment that separates them into three distinct subspecies accurately reflects their distinct evolutionary potentials.…”

“…Although this difference can be explained as nuclear markers coalesce four times more slowly than plastid markers due to biparental inheritance (Moore, 1995), gene flow between these groups has likely continued due to artificial transplanting as a means of population augmentation (USFWS, 1993). Nevertheless, the lineage separation based on plastid sequences likely resulted from the highly disjunctive and fragmented distributions of American populations as they have persisted in geographically isolated climatic refugia since the Pleistocene (Watkins & Farrar, 2005;Heo & al., 2022). Genetic drift, particularly in the small southern populations (e.g., Alabama), has likely facilitated divergences and thus necessitates more geographically refined ESUs as the operational conservation units for reintroduction or augmentation programs to preserve long-term genetic distinctiveness (Moritz, 1994).…”

“…americanum and A. komarovii . A high degree of geographic segregation due to historical vicariance events (e.g., disappearance of the Bering land bridge) may have led to geographically/taxonomically independent reproduction (Heo & al., 2022). Consequently, A. komarovii should be reclassified as an infraspecies of A. scolopendrium .…”

“…scolopendrium , 7 for A. scolopendrium var. americanum , 6 for A. komarovii ), and compared with markers based on widely used plastid DNA regions ( rbcL , trnL‐trnF , atpB‐rbcL ) sequenced in a previous study (Heo & al., 2022). Discrimination accuracy was estimated as the number of taxa in the generated phylogenetic trees that are accurately assigned to their corresponding regional monophyletic groups.…”