Genomic Differentiation and Demographic Histories of Two Closely Related Salicaceae Species

Abstract

Populus alba (P. alba) and Populus davidiana (P. davidiana) are important plant species for answering a variety of issues on species evolution due to their wide distribution and ability to adapt to a variety of environments and climates. Even though P. alba and P. davidiana belong to ecologically and economically important forest trees in the Northern Hemisphere, little is known about their genomic landscape and genome divergence during speciation. We re-sequenced 20 and 19 members of P. davidiana and P. alba, respectively, and found that the Dxy value between P. alba and P. davidiana was 0.2658, whereas the F _ST values were 0.2988, indicating that the genetic divergence was fairly clear. Populus davidiana and P. alba diverged from the ancestor in the middle Pleistocene, c. 0.80 Ma (95% HPD: 0.79-0.81 Ma). The population sizes of P. davidiana increased ~20,000 years ago after a considerable long-term decline following divergence. However, after differentiation, the effective population size of P. alba expanded slightly before experiencing a long-term bottleneck effect. According to the expectation of allopatric speciation, we found a significant number of genomic differentiation sites in both species' speciation events, and the majority of these genomic differentiation regions can be attributed to neutral evolutionary processes. Nevertheless, the regions with extreme divergence exist in abundance, indicating that natural selection has had an impact. Positive selection can be found in highly differentiated regions, while long-term balancing selection traits can be easily observed in low differentiated regions. According to these findings, climate differences over the Quaternary, as well as variance in linked selection and recombination, all contributed significantly to genomic divergence during allopatric speciation of the two aspens.

Keywords: adaptation; demographic history; genetic diversity; natural selection; whole-genome sequencing.

Figure 1

Genetic structure of 20 Populus davidiana and 19 Populus alba. (A) Genetic structure of P. davidiana and P. alba inferred using NGSadmix. (B) A rooted neighbor-joining tree constructed from the allele-shared matrix of SNPs among the P. davidiana and P. alba. (C) Principal component analysis (PCA) plot based on genetic covariance. (D) Pie chart summarizing the proportion of fixed, shared and exclusive polymorphisms of the two species.

Figure 2

(A) Best-fitting model inferred demographic histories and differentiation mode for Populus davidiana and P. alba implemented by fastsimcoal 2.6.1. (B) The effective population size (Ne) over historical time implementing by PSMC.

Figure 3

Linkage disequilibrium decay patterns for P. davidiana and P. alba.

Figure 4

Comparisons of dxy (A), RND (B), and shared (C) among regions displaying significantly high (yellow boxes) and low (red boxes) differentiation vs. the genomic background (blue boxes) between P. davidiana and P. alba. Asterisks designate significant differences between outlier windows and the rest of genomic regions by Mann-Whitney U test (***P-value < 2.2e–16).

Figure 5

The outlier regions are significantly influenced by natural selection. (A,B) Comparisons of nucleotide diversity π among regions displaying significantly high (yellow boxes) and low (red boxes) differentiation vs. the genomic background (blue boxes) between P. davidiana and P. alba.; (C,D) Comparisons of Fay & Wu's H in P. davidiana and P. alba; (E,F) Comparisons of Tajima's D in P. davidiana and P. alba; (G,H) Comparisons of r² in P. davidiana and P. alba; (I,J) Comparisons of recombination rate (ρ/θπ) in P. davidiana and P. alba; (K,L) Comparisons of the proportion of fixed differences caused by derived alleles fixed in P. davidiana and P. alba. Asterisks designate significant differences between outlier windows and the rest of genomic regions by Mann-Whitney U test (***P < 2.2e–16).

Figure 6

GO enrichment analysis in highly differentiated regions between P. davidiana and P. alba.

Figure 7

KEGG pathways enrichment analysis in highly differentiated regions between P. davidiana and P. alba.