Genomic insights on the contribution of balancing selection and local adaptation to the long‐term survival of a widespread living fossil tree, Cercidiphyllum japonicum

Abstract

Summary ‘Living fossils’ are testimonies of long‐term sustained ecological success, but how demographic history and natural selection contributed to their survival, resilience, and persistence in the face of Quaternary climate fluctuations remains unclear. To better understand the interplay between demographic history and selection in shaping genomic diversity and evolution of such organisms, we assembled the whole genome of Cercidiphyllum japonicum, a widespread East Asian Tertiary relict tree, and resequenced 99 individuals of C. japonicum and its sister species, Cercidiphyllum magnificum (Central Japan). We dated this speciation event to the mid‐Miocene, and the intraspecific lineage divergence of C. japonicum (China vs Japan) to the Early Pliocene. Throughout climatic upheavals of the late Tertiary/Quaternary, population bottlenecks greatly reduced the genetic diversity of C. japonicum. However, this polymorphism loss was likely counteracted by, first, long‐term balancing selection at multiple chromosomal and heterozygous gene regions, potentially reflecting overdominance, and, second, selective sweeps at stress response and growth‐related genes likely involved in local adaptation. Our findings contribute to a better understanding of how living fossils have survived climatic upheaval and maintained an extensive geographic range; that is, both types of selection could be major factors contributing to the species' survival, resilience, and persistence.

A test of the centre–periphery hypothesis using population genetics in an East Asian Tertiary relict tree

“…All priors were generated with R 3.5.1 (R Development Core Team, 2018) and the population size change scenarios were simulated 10,000 times by fastsimcoal2 2.5.2 (Excoffier & Foll, 2011). Following Zhu et al, (2020), eight summary statistics, including averages and standard deviations of four parameters (number of alleles, expected heterozygosity, allele size range and Garza–Williamson index), were calculated for observed and simulated data using arlsumstat 3.5.2 (Excoffier & Lischer, 2010). Then, to compare the five models, we adopted an ABC random forest (ABC‐RF) approach implemented in the R package abcrf 1.7 (Pudlo et al, 2015).…”

Landscape Genomics in Tree Conservation Under a Changing Environment

“…However, the number of SNPs obtained and the ability to detect genes underlying local adaptation from the abovementioned methods may be influenced due to the differences in library preparation, SNP densities, and the bioinformatics parameters applied to SNP filtering ( Hoban et al, 2016 ; Lowry et al, 2017 ; McKinney et al, 2017 ). As more and more forest tree genomes have been published (e.g., Table 1 in Ingvarsson et al, 2016 ) and sequencing costs fall, whole-genome resequencing is thriving and becoming an option for landscape genomics studies ( Lin et al, 2018 ; Zhu et al, 2020 ), which can provide unprecedented marker density and determine other genetic variation such as structural variants and mutations in regulatory elements, increasing power for the detection of local adaptation and providing novel insights into the role of selection, recombination, and gene flow in promoting or impairing local adaptation to new habitats compared with reduced-representation methods ( Fuentes-Pardo and Ruzzante, 2017 ; Bourgeois and Warren, 2021 ). In addition, the degrees of linkage disequilibrium (LD) in the studied species will also influence the power of detecting adaptive SNPs.…”

The global significance of biodiversity science in China: an overview

“…Recent studies revealed at least five cryptic phylogenetic species in Chinese giant salamanders ( Andrias davidianus ) [ 142 ] and two phylogenetic species in red pandas [ 143 ], which require subsequent lineage-specific conservation strategies. Consistent with their small population sizes, the threatened Baiji river dolphin, Myanmar snub-nosed monkey ( Rhinopithecus strykeri ), Himalayan red panda ( Ailurus fulgens ), ironwood tree ( Ostrya rehderiana ) and Cercidiphyllum japonicum [ 144 ] had very low genetic diversities [ 143 , 145 , 146 ]. Crested ibis ( Nipponia nippon ) populations have lost almost half of their ancestral genetic diversity [ 147 ].…”