Gene flow, linked selection, and divergent sorting of ancient polymorphism shape genomic divergence landscape in a group of edaphic specialists

Abstract

Interpreting the formation of genomic variation landscape, especially genomic regions with elevated differentiation (i.e. islands), is fundamental to a better understanding of the genomic consequences of adaptation and speciation. Edaphic islands provide excellent systems for understanding the interplay of gene flow and selection in driving population divergence and speciation. However, discerning the relative contribution of these factors that modify patterns of genomic variation remains difficult. We analysed 132 genomes from five recently divergent species in Primulina genus, with four species distributed in Karst limestone habitats and the fifth one growing in Danxia habitats. We demonstrated that both gene flow and linked selection have contributed to genome‐wide variation landscape, where genomic regions with elevated differentiation (i.e., islands) were largely derived by divergent sorting of ancient polymorphism. Specifically, we identified several lineage‐specific genomic islands that might have facilitated adaptation of P. suichuanensis to Danxia habitats. Our study is amongst the first cases disentangling evolutionary processes that shape genomic variation of plant specialists, and demonstrates the important role of ancient polymorphism in the formation of genomic islands that potentially mediate adaptation and speciation of endemic plants in special soil habitats.

Linked selection, differential introgression and recombination rate variation promote heterogeneous divergence in a pair of yellow croakers

“…This result is similar to the observations in Ficedula flycatchers (Burri et al, 2015), Darwin's finches (Vijay et al, 2017) and Primulina species (Ke et al, 2022), where the shared patterns of heterogeneous genomic landscapes between species or lineages are contributed by linked selection in low recombination regions.…”

“…Divergent sorting of ancient haplotypes after the onset of speciation is common and predicted to elevate D xy and have reduced lineagespecific genetic measures (ρ, π and Tajima's D) in genomic islands (Han et al, 2017;Ke et al, 2022;Ma et al, 2018). Under this scenario, global patterns of positive correlations between F ST and D xy , between genetic diversity and D xy , and between recombination rate and D xy , are also expected (Ke et al, 2022;Ma et al, 2018;Wang et al, 2019).…”

Phylogeographic structure of Heteroplexis (Asteraceae), an endangered endemic genus in the limestone karst regions of southern China

“…In this case, Ne was maintained at a steady state during the LGP for all Heteroplexis species, indicating that migration was effective in stabilizing populations. The response of Heteroplexis to the LGP is similar to those of such genera as Cycas ( Tao et al., 2021 ), Primulina ( Ke et al., 2022 ), and Rhododendron ( Zhang et al., 2021b ), suggesting that the karst mountains in Guangxi may be a glacial refugium for Heteroplexis . It is suggested to reconstruct the biogeographic history of Heteroplexis at a finer genomic scale and incorporate other evidence, such as fossil information ( Yan et al., 2021 ), to test the above mentioned hypothesis.…”

“…One possible explanation is that these gene flow events occurred at the beginning of species divergence, when the Heteroplexis ancestors had a wider range than today for gene flow. However, geological activities and climate change led to the present fragmented populations ( Zhang et al., 2021b ; Ke et al., 2022 ). In addition, if current allopatric species have experienced migration events, gene flow events may have taken place when they were sympatric ( Sun et al., 2015 ).…”

“…The population size of Heteroplexis is lower in densely vegetated habitats than in sparsely vegetated habitats (e.g., bare rocks). According to previous studies, the climate has stabilized after entering the Holocene, and the populations of many species have been gradually recovering or exploding ( Miao et al., 2021 ; Ke et al., 2022 ). We speculate that the population recovery of other species has led to a smaller ecological niche of Heteroplexis species and thereby a smaller size of their population.…”