长江下游外来生物福寿螺的种类及其种群遗传结构

doi:10.17520/biods.2022346

生物多样性 ›› 2023, Vol. 31 ›› Issue (3): 22346. DOI: 10.17520/biods.2022346

所属专题：生物入侵

• 研究报告: 遗传多样性 • 上一篇下一篇

长江下游外来生物福寿螺的种类及其种群遗传结构

蒲佳佳¹, 杨平俊², 戴洋³, 陶可欣¹, 高磊⁴, 杜予州⁵, 曹俊³, 俞晓平¹, 杨倩倩¹^,^*()

1.中国计量大学生命科学学院, 浙江省生物计量及检验检疫技术重点实验室, 杭州 310018
2.苏州市植物保护植物检疫站, 江苏苏州 215128
3.江苏省血吸虫病防治研究所, 江苏无锡 214064
4.上海市园林科学规划研究院, 上海 200232
5.扬州大学园艺与植物保护学院, 江苏扬州 225009

收稿日期:2022-06-24 接受日期:2022-09-05 出版日期:2023-03-20 发布日期:2022-12-30
通讯作者: 杨倩倩
作者简介:* E-mail: yqq@cjlu.edu.cn
基金资助:
国家重点研发计划(2020YFC1200100);国家自然科学基金(32171668);国家留学基金委促进与加澳新拉美地区科研合作与高层次人才培养项目和浙江省属高校基本科研业务费专项资金(2021YW06)

Species identification and population genetic structure of non-native apple snails (Ampullariidea: Pomacea) in the lower reaches of the Yangtze River

Jiajia Pu¹, Pingjun Yang², Yang Dai³, Kexin Tao¹, Lei Gao⁴, Yuzhou Du⁵, Jun Cao³, Xiaoping Yu¹, Qianqian Yang¹^,^*()

1 Zhejiang Provincial Key Laboratory of Biometrology and Inspection & Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018
2 Suzhou Station of Plant Protection and Plant Quarantine, Suzhou, Jiangsu 215128
3 Jiangsu Institute of Parasitic Diseases, Wuxi, Jiangsu 214064
4 Shanghai Academy of Landscape Architecture Science and Planning, Shanghai 200232
5 School of Horticulture and Plant Protection, Yangzhou University, Yangzhou, Jiangsu 225009

Received:2022-06-24 Accepted:2022-09-05 Online:2023-03-20 Published:2022-12-30
Contact: Qianqian Yang

摘要/Abstract

摘要：

福寿螺(Pomacea spp.)已广泛分布在我国长江以南各省, 且逐年向北扩散。本研究采集了长江下游上海及江苏分布区11个种群的福寿螺样品, 测序获得270条线粒体COI基因序列, 生成10个单倍型(Hap1-10)。基于遗传距离及系统发育分析将Hap1-9鉴定为小管福寿螺(Pomacea canaliculata), Hap10为斑点福寿螺(P. maculata)。其中, 小管福寿螺在所有采样点均有分布; AMOVA层次分析将小管福寿螺种群分成跨长江分布的3个组群, 且分子变异主要来源于组群间。进一步结合已发表的我国其他地区(大陆和香港), 以及日本和原产地阿根廷、巴西种群的福寿螺序列, 形成包含972条COI序列的数据集进行种群遗传学分析。单倍型网络分析中, 所采集的小管福寿螺种群分布于3个包含阿根廷单倍型的子网络, 其中包含Hap5和Hap7的子网络在我国首次被发现, 表明长江下游地区小管福寿螺从阿根廷多次入侵, 并发现一个新的入侵历史事件。斑点福寿螺仅在长江以北江苏地区检测到, 单倍型Hap10也是我国大陆其他地区的主要单倍型, 表明长江以北江苏地区的斑点福寿螺可能由国内已有分布区扩散而来, 均起源于巴西。我国不同地区种群的遗传多样性比较发现, 长江以南的小管福寿螺遗传多样性最高(Hd = 0.627), 而香港种群斑点福寿螺的遗传多样性最高(Hd = 0.356)。基于核EF1α基因分型分析检测表明, 所采集福寿螺的杂交种比例为52.6%, 高于原产地种群, 表明种间渐渗杂交在入侵过程中持续发生。本研究对于福寿螺监测预警及有效防控具有重要意义。

关键词: 生物入侵, 分子鉴定, 种群遗传多样性, COI, 渐渗杂交, 扩散

Abstract

Aims: Apple snails (Pomacea spp.) distribute widely in the Chinese provinces south of the Yangtze River, which are spreading to the northern regions every year. We aimed to determine the identities and distributions of Pomacea species in the lower reaches of the Yangtze River.

Methods: In this study, we collected apple snail samples from 11 populations in Shanghai and Jiangsu Province at the lower reaches of the Yangtze River. From these samples, we sequenced 270 mitochondrial COI sequences. We retrieved the published Pomacea sequences of other Chinese populations (in the China’s mainland and Hong Kong), Japanese populations, and the native populations in Argentina and Brazil to form a COI dataset of 972 sequences from GenBank. We first identified species based on genetic distance and phylogenetic analysis of haplotypes and then analyzed the population genetic structures based on the parsimony network under 95% parsimony limit using the COI dataset. To compare the genetic diversity of the populations from this study and other Chinese populations, we calculated the haplotype diversity (Hd), nucleotide diversity (π), and average number of nucleotide difference (k) for the populations of P. canaliculata and P. maculata. We conducted the hierarchical analysis of molecular variance (AMOVA) of the populations from the south and north of the Yangtze River for P. canaliculata, due to only this species distributed in both banks. Finally, we determined the introgression patterns by genotyping the nuclear EF1α using the primer-specific- multiplex polymerase chain reaction (PCR).

Results: We generated 10 haplotypes (Hap1-10) from the COI dataset, and identified Hap1-9 as P. canaliculata, and Hap10 as P. maculata. Pomacea canaliculata was found in all the surveyed populations, while P. maculata was only found in the Jiangsu populations north of the Yangtze River. The parsimony network of the populations of P. canaliculata split into three sub-networks, and each shared the haplotypes from Argentina. Notably, the sub-network containing Hap5 and Hap7 was firstly discovered in China. Both the parsimony network and the distribution frequencies of the haplotypes revealed that the population structures in this region were similar to the Japanese populations. Hap10 of P. maculata was identical with the dominant haplotype in other regions of China, which was shared with the haplotype from Brazil. The population diversity of P. canaliculata found in this study was the highest compared to other studies (Hd = 0.627), whereas the population diversity of P. maculata from the highest (Hd = 0.356) in Hong Kong. The populations of P. canaliculata across the Yangtze River were divided into three groups by AMOVA analysis, with the major source of molecular variance contributed from the groups. Genotyping the nuclear EF1α gene of the apple snails from this study revealed 52.6% hybrids, which was higher than that of the native populations.

Conclusion: The P. canaliculata populations in the lower reaches of the Yangtze River likely result from multiple introductions from Argentina, and provide a new history of introduction of P. canaliculata in Shanghai and Jiangsu Province. Pomacea maculata may be introduced from other existing populations in China mainly in Sichuan Basin and Zhejiang Province, which are derived originally from Brazil. The high proportion of hybrids suggest continuous introgressive hybridization during the invasion process. Our results provide important information for the monitoring and effective control of invasive apple snails.

Key words: biological invasion, molecular identification, population diversity, mitochondrial COI, introgressive hybridization, spread

蒲佳佳, 杨平俊, 戴洋, 陶可欣, 高磊, 杜予州, 曹俊, 俞晓平, 杨倩倩 (2023) 长江下游外来生物福寿螺的种类及其种群遗传结构. 生物多样性, 31, 22346. DOI: 10.17520/biods.2022346.

Jiajia Pu, Pingjun Yang, Yang Dai, Kexin Tao, Lei Gao, Yuzhou Du, Jun Cao, Xiaoping Yu, Qianqian Yang (2023) Species identification and population genetic structure of non-native apple snails (Ampullariidea: Pomacea) in the lower reaches of the Yangtze River. Biodiversity Science, 31, 22346. DOI: 10.17520/biods.2022346.

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https://www.biodiversity-science.net/CN/Y2023/V31/I3/22346

图/表 10

表1 长江下游分布区福寿螺样品采集信息

Table 1 Sampling information of the apple snails collected from the lower reaches of the Yangtze River

序号 Code	地点 Locality	编号 Code	经度 Longitude (E)	纬度 Latitude (N)	生境 Habitat	序列数量 No. of sequences
1	上海市宝山区三星村 Sanxing Village, Baoshan District, Shanghai	SHBS	121.36°	31.31°	河道 River	20
2	苏州市吴中区甪直镇 Luzhi Town, Wuzhong District, Suzhou City	WZLZ	120.48°	31.14°	水生蔬菜田 Aquatic vegetable field	30
3	苏州市吴中区马家浜村 Majiabang Village, Wuzhong District, Suzhou City	WZMJB	120.46°	31.14°	水生蔬菜田 Aquatic vegetable field	30
4	昆山市周庄镇 Zhouzhuang Town, Kunshan City	KSZZ	120.56°	31.21°	稻田 Paddy field	30
5	常熟市尚湖镇 Shanghu Town, Changshu City	CSSH	120.42°	31.36°	稻田 Paddy field	30
6	常熟市古里镇 Guli Town, Changshu City	CSGL	120.85°	31.65°	稻田 Paddy field	15
7	张家港市凤凰镇鸷山 Fenghuang Town, Zhangjiagang City	ZJGFH	120.62°	31.76°	沟渠 Ditch	17
8	张家港市凤凰镇杏市村 Xingshi Village, Fenghuang Town, Zhangjiagang City	ZJGXSC	120.68°	31.78°	稻田 Paddy field	28
9	扬州市广陵区沙头镇 Shatou Town, Guangling District, Yangzhou City	JSYZ	119.50°	32.34°	河道 River	30
10	泰州市兴化市大邹镇顾马村 Guma Village, Dazou Town, Xinghua City, Taizhou City	JSTZ	119.92°	33.15°	河道、蟹田 River, crab field	30
11	宿迁市泗洪县 Sihong County, Suqian City	JSSQ	118.25°	33.47°	湖泊 Lake	10

图1 本研究福寿螺采样点及基于AMOVA层次分析的分组。实心圆表示采样点, 同一线型框表示同一组群, 图中缩写含义见表1。

Fig. 1 Sampling locations of the apple snails and grouping based on AMOVA hierarchical analysis. Solid circles represent sampling points, the frames in same linetype indicates a population group, the meaning of the abbreviation in the figure is shown in Table 1.

图2 基于K2P遗传距离的单倍型序列相似性热图。P. canaliculata: 小管福寿螺; P. maculata: 斑点福寿螺; P. occulta: 隐秘福寿螺。

Fig. 2 Heatmap of the sequence similarities based on K2P genetic distance of the haplotypes

图3 长江下游福寿螺单倍型构建的系统发育树。系统发育分支节点为相邻连接法/贝叶斯法(NJ/BI)系统发育树的置信值, 仅显示> 60%的数值; 其中加粗显示的Hap1?10为本研究所测COI序列生成的单倍型。

Fig. 3 The phylogenetic tree constructed by the haplotypes of apple snails from the lower reaches of the Yangtze River. The branch nodes of phylogenetic trees denote neighbor-joining/ Bayesian inference bootstrap supports. Only the values > 60% are displayed; Hap1-10 shown in bold are haplotypes generated from COI sequences from this study.

表2 本研究福寿螺种群的COI单倍型分布。地点编号见表1。

Table 2 Distribution of COI haplotypes of the populations from this study. Location code see Table 1.

单倍型 Haplotype	序列数量 No. of sequences (%)	SHBS	WZLZ	WZMJB	KSZZ	CSSH	CSGL	ZJGFH	ZJGXSC	JSYZ	JSTZ	JSSQ	物种 Species
Hap1	126 (46.67)	19	23	16	30	27	-	-	-	-	2	9	小管福寿螺Pomacea canaliculata
Hap2	15 (5.56)	-	-	-	-	-	-	10	-	-	5	-	小管福寿螺 P. canaliculata
Hap3	21 (7.78)	-	-	-	-	-	15	6	-	-	-	-	小管福寿螺 P. canaliculata
Hap4	28 (10.37)	-	-	-	-	-	-	-	28	-	-	-	小管福寿螺 P. canaliculata
Hap5	22 (8.15)	-	7	14	-	1	-	-	-	-	-	-	小管福寿螺 P. canaliculata
Hap6	18 (6.67)	-	-	-	-	-	-	-	-	18	-	-	小管福寿螺 P. canaliculata
Hap7	1 (0.37)	1	-	-	-	-	-	-	-	-			小管福寿螺 P. canaliculata
Hap8	2 (0.74)	-	-	-	-	2	-	-	-	-			小管福寿螺 P. canaliculata
Hap9	1 (0.37)	-	-	-	-	-	-	1	-	-	-	-	小管福寿螺 P. canaliculata
Hap10	36 (13.33)	-	-	-	-	-	-	-	-	12	23	1	斑点福寿螺 P. maculata

图4 基于TCS模型建立的小管福寿螺单倍型网络。95%简约连接界限下分成4个子网络(A?D); 圆的大小与序列量成正比, 不同图案代表不同地理种群, 白色圆表示缺失单倍型。

Fig. 4 Haplotype network of Pomacea canaliculata based on TCS model. The haplotypes network of P. canaliculata splits into four sub-networks (A?D) under 95% parsimony limit. The size of the circles represents the number of sequences. Pattern types represent different geographical populations, with the white circles indicating missing haplotypes.

图5 基于TCS模型建立的斑点福寿螺单倍型网络。95%简约连接界限下分成7个子网络(A?G); 圆的大小与序列量成正比, 不同图案代表不同地理种群, 白色圆表示缺失单倍型。

Fig. 5 Haplotype network of Pomacea maculata based on TCS model. The haplotypes network of P. maculata splits into seven sub-networks (A?G) under 95% parsimony limit. The size of the circles represents the number of sequences. Pattern types represent different geographical populations, with the white circles indicating missing haplotypes.

表3 本研究种群、已发表的中国大陆及香港种群的小管福寿螺和斑点福寿螺的遗传多样性

Table 3 Distribution of population genetic diversity of Pomacea canaliculata and P. maculata from this study, published by China’s mainland and Hong Kong, and this study

物种 Species	地理种群 Region	序列数 No. of sequences	单倍型数 No. of haplotypes	单倍型多样性 Haplotype diversity (Hd)	核苷酸多样性 Nucleotide diversity (π)	核苷酸平均差异数 Average number of nucleotide difference (k)
小管福寿螺 Pomacea canaliculata	长江以南 South of the Yangtze River	200	8	0.627	0.02546	14.744
	长江以北 North of the Yangtze River	34	3	0.611	0.02541	14.713
	中国大陆已发表 Published by China’s mainland	319	7	0.587	0.02543	14.722
	香港 Hong Kong	139	5	0.441	0.01956	11.324
斑点福寿螺 P. maculata	江苏 Jiangsu	36	1	0.000	0.00000	0.000
	中国大陆已发表 Published by China’s mainland	30	2	0.067	0.00035	0.200
	香港 Hong Kong	10	2	0.356	0.00430	2.489

表4 长江下游分布区小管福寿螺种群COI分子变异方差分析

Table 4 Variance analysis of COI molecular variation among populations of Pomacea canaliculata in the lower reaches of the Yangtze River

变异来源 Source of variation	自由度 Degree of freedom	平方和 Sum of squares	方差组分 Variance components	变异百分率 Percentage of variation (%)
组群间 Among groups	2	122.265	9.56034	7.37
组群内种群间 Among populations within groups	8	165.622	0.89486	7.24
种群内个体间 Among individuals within populations	223	423.865	1.90074	15.38
总变异 Total variation	233	1,811.752	12.35594	100.00

图6 基于核EF1α基因多重PCR扩增的长江下游福寿螺杂交渐渗型检测。M为50 bp DNA梯带; 1?6为长江下游福寿螺样品, 分别为M型、B型、C型、C型、C型、B型。

Fig. 6 Introgressive hybridization of the apple snails in the lower reaches of the Yangtze River based on EF1α gene multiplex PCR method. M, 50 bp DNA ladder; 1?6 represent for M type, B type, C type, C type, C type, and B type of samples of apple snails collected in the lower reaches of the Yangtze River.

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长江下游外来生物福寿螺的种类及其种群遗传结构

Species identification and population genetic structure of non-native apple snails (Ampullariidea: Pomacea) in the lower reaches of the Yangtze River

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