Ginkgo biloba’s footprint of dynamic Pleistocene history dates back only 390,000 years ago

Abstract

BackgroundAt the end of the Pliocene and the beginning of Pleistocene glaciation and deglaciation cycles Ginkgo biloba went extinct all over the world, and only few populations remained in China in relict areas serving as sanctuary for Tertiary relict trees. Yet the status of these regions as refuge areas with naturally existing populations has been proven not earlier than one decade ago. Herein we elaborated the hypothesis that during the Pleistocene cooling periods G. biloba expanded its distribution range in China repeatedly. Whole plastid genomes were sequenced, assembled and annotated, and sequence data was analyzed in a phylogenetic framework of the entire gymnosperms to establish a robust spatio-temporal framework for gymnosperms and in particular for G. biloba Pleistocene evolutionary history.ResultsUsing a phylogenetic approach, we identified that Ginkgoatae stem group age is about 325 million years, whereas crown group radiation of extant Ginkgo started not earlier than 390,000 years ago. During repeated warming phases, Gingko populations were separated and isolated by contraction of distribution range and retreated into mountainous regions serving as refuge for warm-temperate deciduous forests. Diversification and phylogenetic splits correlate with the onset of cooling phases when Ginkgo expanded its distribution range and gene pools merged.ConclusionsAnalysis of whole plastid genome sequence data representing the entire spatio-temporal genetic variation of wild extant Ginkgo populations revealed the deepest temporal footprint dating back to approximately 390,000 years ago. Present-day directional West-East admixture of genetic diversity is shown to be the result of pronounced effects of the last cooling period. Our evolutionary framework will serve as a conceptual roadmap for forthcoming genomic sequence data, which can then provide deep insights into the demographic history of Ginkgo.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4673-2) contains supplementary material, which is available to authorized users.

Phylogenomics supports a Cenozoic rediversification of the “living fossil” Isoetes

“…Despite morphological stasis, Isoetes recently expanded Our results are consistent with an increasing number of studies in groups such as cycads [13], bryophytes [27] and Ginkgo [26] showing relatively recent origins of extant species of these 585 groups, despite long periods of morphological stasis.…”

“…Analyses of DNA sequences over the last few decades have resolved the phylogenetic relationships between many extant lineages, and large numbers of selectively neutral changes in the genomes allowed inferring accurate phylogenies even for the most morphologically uniform organisms [21,22]. Molecular divergence in parts of the tree with informative fossils 65 can then be used to time-calibrate molecular changes in the rest of the tree, allowing inference of divergence times of groups of organisms lacking an appropriate fossil record [23][24][25][26]. This molecular dating technique has been used to investigate the evolutionary dynamics of some "living fossil" groups, which in some cases indeed showed ancient within-group divergence and extant distributions resulting from continental drift tens of millions of years ago [17].…”

“…This molecular dating technique has been used to investigate the evolutionary dynamics of some "living fossil" groups, which in some cases indeed showed ancient within-group divergence and extant distributions resulting from continental drift tens of millions of years ago [17]. In 70 groups such as cycads [13], bryophytes [27] and Ginkgo [26], however, extant diversity originated more recently than their conserved morphology would suggest, indicating complex evolutionary dynamics for some "living fossil" taxa. Age estimates from molecular dating techniques remain however sensitive to the treatment of fossil data, variability in the rates of nucleotide substitutions between molecular markers and species, and the correct alignment of 75 nucleotide markers [24,[28][29][30][31][32][33].…”

Phylogenomics indicates the “living fossil” Isoetes diversified in the Cenozoic

“…Analyses of DNA sequences over the last few decades have resolved the phylogenetic relationships between many extant lineages, and large numbers of selectively neutral changes in the genomes allowed inferring accurate phylogenies even for the most morphologically uniform organisms [21,22]. Molecular divergence in parts of the tree with informative fossils can then be used to time-calibrate molecular changes in the rest of the tree, allowing inference of divergence times of groups of organisms lacking an appropriate fossil record [23][24][25][26]. This molecular dating technique, alongside other methods, has been used to investigate the evolutionary dynamics of some "living fossil" groups.…”

Predicting the Bioclimatic Habitat Suitability of Ginkgo biloba L. in China with Field-Test Validations

“…First, the long-lived tree will be unlikely to migrate fast enough to avoid the negative effects of climate change. Second, the characteristics of shade intolerance, late reproductive maturity (approximately 20 years), clonal propagation of secondary trunks, and large seeds may be unfavorable to the migration of ginkgo populations [16][17][18][19]. Presumably, ginkgo may be in danger of extinction in some habitats if it fails to adapt to rapid climate change in the future.…”