Genomic analyses provide new insights into the evolutionary history and reproduction of the Paleogene relictual Kingdonia (Circaeasteraceae, Ranunculales)

Abstract

AbstractAsexual lineages are perceived to be short-lived on evolutionary timescales due to accumulation of deleterious mutations. Hence reports for exceptional cases of putative ‘ancient asexual’ species usually raise doubts about whether such species are recently derived or engage in some undocumented sexual reproduction. However, there have been few studies to solve the mystery. The monotypic Kingdonia dating to the early Eocene, contains only K. uniflora that has no known definitive evidence for sexual reproduction nor records for having closely related congeneric sexual species, seeming to have persisted under strict asexuality for long periods of time. In this study, we use population genomic analyses to test for reproduction mode and infer the evolutionary process and mechanisms facilitating the survival of the species. Our results indicate the presence of three differentiating genetic lineages within the species and support that asexual reproduction in K. uniflora indicated by high allelic heterozygosity had occurred prior to the lineage differentiation (∼0.5 mya). We also detected DNA recombination events in some populations, in line with occurrence of unseen and unevenly distributed sexual reproduction among populations. However the observation of high linkage disequilibrium, relatively high ratio of πN/πS (nonsynonymous versus synonymous nucleotide diversity), together with high allelic heterozygosity suggest the sexual reproduction is infrequent. Furthermore, we found that genes containing SNPs with elevated Fst values are significantly enriched in functions associated with seed development, suggesting differentiation in genes regulating seed development is likely to be the key reason of the uneven distribution of sexual reproduction in K. uniflora. Evidence from our study supports predominate asexual reproduction in K. uniflora, but unseen sexual reproduction must have played a key role to ensure the long-term survival of the lineage in general. Uneven distribution of sexual reproduction in the species may be a key factor underlying the observed genetic differentiation between populations. This study provides novel insights into the reproduction and evolution of Kingdonia, a relict lineage evolved in the Paleogene and known for asexual reproduction, and demonstrate the power of data from population genome sequencing in resolving long-standing evolutionary questions.