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. 2023 Jan 18;44(1):3-19.
doi: 10.24272/j.issn.2095-8137.2022.108.

A wide hybrid zone mediated by precipitation contributed to confused geographical structure of Scutiger boulengeri

Xiu-Qin Lin  1   2 , Yin-Meng Hou  1   2 , Wei-Zhao Yang  1   2 , Sheng-Chao Shi  1   2 , Pu-Yang Zheng  1   2 , Chung-Kun Shih  3   4 , Jian-Ping Jiang  1   2   5 , Feng Xie  1   2   6
Affiliations

A wide hybrid zone mediated by precipitation contributed to confused geographical structure of Scutiger boulengeri

Xiu-Qin Lin et al. Zool Res. .

Abstract
in English, Chinese

Confused geographical structure of a population and mitonuclear discordance are shaped by a combination of rapid changes in population demographics and shifts in ecology. In this study, we generated a time-calibrated phylogeny of Scutiger boulengeri, an endemic Xizang alpine toad occurring in mountain streams on the Qinghai-Xizang (Tibet) Plateau (QTP). Based on three mitochondrial DNA (mtDNA) genes, eight clades were assigned to three deeply divergent lineages. Analysis of nuclear DNA (nuDNA) genes revealed three distinct clusters without geographic structure, indicating significantly high rates of gene flow. Coalescent theory framework analysis (approximate Bayesian computation model DIYABC and Migrate-N) suggested that divergence of the main intraspecific clusters was the result of hybridization after secondary contact in the Holocene around 0.59 million years ago (Ma). The ratio of mtDNA F ST (fixation index) to nuDNA F ST was 2.3, thus failing to show male-biased dispersal. Geographic cline analysis showed that a wide hybrid zone was initially established in southwestern China, without significant reproductive isolation but with strong introgression in S. boulengeri, suggesting high hybrid fitness. Furthermore, mtDNA genes exhibited isolation by distance (IBD) while nuDNA genes exhibited significant isolation by environment (IBE). Results suggested that mitonuclear discordance may have initially been caused by geographic isolation, followed by precipitation-mediated hybridization, producing a wide hybrid zone and geographic structure confusion of nuDNA genes in S. boulengeri. This study indicated that complicated historical processes may have led to specific genetic patterns, with a specific climate factor facilitating gene flow in the system.

混乱的种群地理结构和线粒体-核基因分化不一致 (Mitonuclear discordance) 是由快速的种群动态变化和生态转移共同影响的结果。该研究基于3个线粒体基因，对青藏高原山地溪流中特有的西藏齿突蟾 ( Scutiger boulengeri) 进行了时间校准的系统发育分析，发现共存在8个小支系分别被归入3个深度分化的遗传支系中，具有明显的地理结构；基于4个核基因对其遗传结构分析，发现该蟾种内存在三个完全不同的群体结构，且群体间存在高频基因流，但没有明显的地理结构。基于一致性理论 (Coalescent theory)近似贝叶斯模型 (DIYABC和Migration-N) 分析，发现种内群体结构分化是由祖先群体经过地理隔离（早更新世，约2.49 Ma）后初步分化的2个群体的部分个体由于气候波动发生二次接触且杂交（全新世，约0.59 Ma）产生第3个群体后代，该历程伴随种群大小的变化。线粒体基因遗传分化指数 ( F ST) 与核基因 F ST的比值为2.3，未检测出偏雄性扩散。地理渐变 (Geographic cline) 分析显示该蟾在中国西南地区（横断山附近）建立了一个宽阔的杂交带（渐变宽度277.63 km），群体间具有明显的杂交渐渗，且不存在明显的生殖隔离，表明该杂交种可能具有较高的适合度。此外，该研究结果表明线粒体基因 (mtDNA) 表现为地理隔离 (Isolation by distance, IBD)，而核基因 (nuDNA) 表现为环境隔离 (Isolation by environment, IBE)，对该线粒体-核基因分化不一致推测群体分化首先是由地理隔离引起的，然后由降雨介导的杂交产生了宽阔的杂交带，这导致了西藏齿突蟾核基因较混乱的地理结构。该研究揭示了西藏齿突蟾复杂的种群历史动态，由特定气候因素促进了该系统内的基因流动，最终导致了该物种特有的遗传模式。.

Keywords: Genetic structure; Hybrid zone; Mitonuclear discordance; Precipitation; Secondary contact.

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Figures

Figure 1
Figure 1
Time-calibrated phylogeny based on mitochondrial DNA and distribution of sampling sites
Figure 2
Figure 2
Geographic distribution regions and genetic structure analyses
Figure 3
Figure 3
Network analysis implemented in SplitsTree4 v4.12
Figure 4
Figure 4
Graphical representation of models evaluated in Migrate-N and models fit using Bayes Factors (Table 2)
Figure 5
Figure 5
Divergent models based on existing assumptions in S. boulengeri and corresponding posterior probabilities for best-selected model in DIYABC analysis
Figure 6
Figure 6
Ideal population historical demographic model and geographic cline analysis
Figure 7
Figure 7
Scatterplots based on Mantel tests
See this image and copyright information in PMC

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