Mechanisms Underlying The Formation Of Genomic Islands Of Divergence Between Ficus Pumila Var.pumila And Ficus Pumila Var.awkeotsang

Uncovering the mechanisms of speciation is an important task in ecological and evolutionary research,and one of the long-debated topics is whether speciation can occur in the presence of gene flow.With the rapid development of sequencing technology during the last two decades,a growing number of studies have revealed a heterogeneous genomic landscape of divergence with the existence of genomic islands of divergence(GIs)between closely related taxa.This pattern was often explained by divergent selection in the presence of gene flow,an evolutionary process emphasized by the speciation-with-gene-flow model(SGFM).However,GIs can also arise from other evolutionary processes,such as introgression,divergent sorting of ancient polymorphisms,recent selective sweep and long-term linked selection.Previous empirical studies often neglected the roles of these evolutionary processes when discerning the mechanisms contributing to GIs.As a consequence,the drawn conclusions are usually less credible,and evidences for SGFM in some previous cases are thought to be inappropriate by later studies.Two varieties of Ficus pumila,i.e.,F.pumila var.pumila(FPP)and F.pumila var.awkeotsang(FPA),differ in many aspects,such as morphology and habitat preference.Meanwhile,some evidences indicate that a certain level of gene flow still exists between them,and therefore,they may represent a promising system for testing SGFM.In addition,previous studies have found introgression between FPP and F.sarmentosa(FS).In this study,using whole-genome resequencing data of FPP,FPA and FS,I first conducted analyses of population structure,introgression,and population demography.Then,I identified GIs between FPP and FPA and compared the properties of GIs with genomic background(GB).The main results are shown below:1)FPP and FPA could be genetically separated according to Admixture,PCA,and phylogenetic tree analysis.ABBA-BABA test indicated that FS shared more derived alleles with FPA than with FPP,suggesting stronger introgression between FS and FPA.FPP and FPA diverged about 3.43 million years ago with continuous asymmetric gene flow,and stronger gene flow was dectected in the direction from FPP to FPA.2)Based on the null distribution of F_ST under different recombination rates according to the best-fitting demographic model,I identified 135 F_ST outlier sliding windows,which were combined into 106 GIs,between FPP and FPA.In contrast to the GB,the GIs were of significantly higher relative node depth,indicating neither recent selective sweep nor long-term linked selection played an important role in GI formation.The GIs were of significantly harder selective sweep,suggesting the phenomenon,that the divergence time of sequence in the GIs was significantly earlier than that between FPP and FPA,might be caused by introgression rather than divergent sorting of ancient polymorphisms.The higher introgression level in GIs also supported the role of introgression.Additionally,FPA populations shared more derived alleles and displayed lower divergence with sympatric than allopatric FPP populations,which were consistent with the prediction of divergent selection in the presence of gene flow.The GO enrichment analysis indicated the GIs were significantly enriched for genes from multiple GO terms involved in pectin metabolism.In conclusion,divergent selection in the presence of gene flow was an important evolutionary process contributing to the formation of GIs between FPP and FPA,thus providing evidence for SGFM.It's worth noting that introgression also played an important role in the formation of GIs.Some favorable genetic variations at divergently selected loci may be introgressed from FS.Previous studies have found pectin methylesterase(PME)plays an important role in plant resistance to heat or cold temperature stress,so the divergent selection in GIs may be related to the adaptation to different ranges of temperature according to the differences in physiological characteristics(PME activity)and habitat preference between FPP and FPA,and the result of GO enrichment analysis.These findings improve our understanding of the long-debated question of whether speciation can occur in the presence of gene flow and also provide an insight for further elucidating the high diversity of Ficus species.