Heterogeneity of synonymous substitution rates in the Xenopus frog genome.

Quintin Lau,Yukako Katsura,Yoko Satta,Takeshi Igawa,Hajime Ogino,Toshimichi Ikemura,Marc Robinson-Rechavi

doi:10.1371/journal.pone.0236515

Abstract

With the increasing availability of high quality genomic data, there is opportunity to deeply explore the genealogical relationships of different gene loci between closely related species. In this study, we utilized genomes of Xenopus laevis (XLA, a tetraploid species with (L) and (S) sub-genomes) and X. tropicalis (XTR, a diploid species) to investigate whether synonymous substitution rates among orthologous or homoeologous genes displayed any heterogeneity. From over 1500 orthologous/homoeologous genes collected, we calculated proportion of synonymous substitutions between genomes/sub-genomes (k) and found variation within and between chromosomes. Within most chromosomes, we identified higher k with distance from the centromere, likely attributed to higher substitution rates and recombination in these regions. Using maximum likelihood methods, we identified further evidence supporting rate heterogeneity, and estimated species divergence times and ancestral population sizes. Estimated species divergence times (XLA.L-XLA.S: ~25.5 mya; XLA-XTR: ~33.0 mya) were slightly younger compared to a past study, attributed to consideration of population size in our study. Meanwhile, we found very large estimated population size in the ancestral populations of the two species (NA = 2.55 x 106). Local hybridization and population structure, which have not yet been well elucidated in frogs, may be a contributing factor to these possible large population sizes.

Highlights

In comparisons between closely related species, it is well considered that different loci within a genome have different genealogical relationships
Genome-wide mean k between genes was lower in the pairwise comparison of XLA.L and XLA.S sub-genomes (k = 0.183 ± 0.043, median = 0.184) compared to inter-species comparisons (k = 0.227 ± 0.055 or 0.235 ± 0.056, median = 0.224 or 0.232) (Table 2). This is expected, since X. tropicalis and X. laevis diverged ~48 mya whereas the two X. laevis sub-genomes diverged ~34 mya [6], and this additional time allowed for increased accumulation of synonymous substitutions
We have demonstrated the presence of synonymous substitution rate heterogeneity within Xenopus frogs at the inter- and intra-chromosomal level

Summary

Introduction

In comparisons between closely related species, it is well considered that different loci within a genome have different genealogical relationships. Many studies have compared several loci in humans with the three great ape species and showed that a majority (46.6–58.5% of loci) support the closest relationship between humans and chimpanzees; other loci support closer genealogical relationships between humans and gorillas or chimpanzees and gorillas [1,2,3]. Such variation in genealogical relationships between different gene loci can be attributed to large ancestral population size and short duration of successive speciation; this large ancestral population size can sometimes be resulting from heterogeneity of mutation.

Methods

Results

Conclusion