牛羊仰口线虫PCR-RFLP鉴别方法的建立及线粒体全基因组序列分析
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摘要
牛仰口线虫(Bunostomum phlebotomum)和羊仰口线虫(Bunostomum trigonocephalum)是寄生于牛、羊小肠内的一类吸血线虫,俗称牛羊钩虫。牛羊感染钩虫会出现贫血、消瘦、生长缓慢、下颌水肿等症状,导致生产性能下降,严重者可引起死亡。仰口线虫病广泛流行于世界各地,每年都有大量的牛、羊感染此病,给畜牧业生产带来很大的经济损失。
先前研究认为钩虫有很强的宿主特异性,一般情况下并不交叉传播。然而,随着研究的不断深入,研究人员发现有些种类的钩虫可以感染多种宿主,如羊仰口线虫主要寄生于绵羊和山羊,但也可感染牛；牛仰口线虫主要寄生于牛,有时也可感染羊。而两种仰口线虫形态十分相似,使得从形态学上准确鉴定虫种难度加大。鉴于此,本研究第一部分内容是在分子水平上建立一种鉴别牛仰口线虫和羊仰口线虫的方法,并以核糖体内转录间隔区(internal transcribed spacer, ITS)序列为基因标记探讨两种仰口线虫的亲缘关系。首先根据已发表的钩口科线虫核糖体DNA (rDNA)核苷酸序列,设计牛仰口线虫和羊仰口线虫rDNA ITS通用引物。分别提取牛仰口线虫和羊仰口线虫的基因组总DNA,进行PCR扩增和测序,获得两种仰口线虫的rDNA ITS序列,通过对ITS序列的酶切位点分析,选用限制性内切酶NdeⅠ对两种虫体的rDNA ITS PCR产物进行酶切,结果发现羊仰口线虫ITSrDNA序列被切成两段,而牛仰口线虫ITS rDNA序列则没有变化,成功建立了鉴别两种线虫的PCR-RFLP方法。该法简单、特异、而且需要DNA量较少,适合临床使用。利用rDNA ITS序列构建的系统发生树显示,牛仰口线虫和羊仰口线虫处于同一分支,亲缘关系较其它钩口科线虫近,但为两种不同的虫种。
由于线粒体DNA(mtDNA)具有进化速度快、基因突变率高、母性遗传等特点,是研究寄生虫系统发生学、群体遗传学和分子分类的理想分子标记。本研究的第二部分内容是研究不同宿主和不同地理来源羊仰口线虫线粒体部分基因序列的遗传多态性。对来自于黑龙江、云南、吉林、陕西四省绵羊和山羊的40条羊仰口线虫成虫样本的线粒体细胞色素c氧化酶亚基Ⅰ(cox1)基因、细胞色素b(cytb)基因、烟酰胺脱氢酶亚基Ⅰ(nad1)基因和亚基Ⅴ(nad5)基因的部分片段进行扩增,应用生物学软件对样本进行多态性分析,结果显示4段线粒体基因的种内变异情况分别为0.5%-1.6%(pcox1)、0.4%-1.7%(pcytb)、0.4%-1.2%(pnadl)和0.2%-1.9%(pnad5),在这4段线粒体部分基因序列中,核苷酸的变异位置大多发生在第三密码子位置,在第一密码子位置和第二密码子位置很少发生变异；与钩口科的犬钩口线虫、十二指肠钩口线虫和美洲板口线虫间的种间差异分别为12.1-14.2%(pcox1)、13.7-16.0%(pcytb)、17.6-19.4%(pnad1)和16.0-21.6%(pnad5),说明羊仰口线虫线粒体各段基因种内变异很小,但种间变异较大。
线粒体基因组学是研究不多但很重要的分子生物学领域。尽管线虫种类繁多,但目前关于线虫线粒体全基因组的研究却相对有限。截止目前,线粒体全基因组被完整或接近完整测序的线虫仅68种,线粒体全基因组的研究资料还相当欠缺。本研究第三部分内容是扩增羊仰口线虫和牛仰口线虫线粒体基因组,对整个基因组序列进行完整测序和序列分析,并基于线粒体基因组蛋白质编码基因序列构建系统发生树,阐明羊仰口线虫、牛仰口线虫与其他线虫的进化关系。本研究采用PCR方法获得的羊仰口线虫和牛仰口线虫线粒体全基因组序列分别为13771bp和13803bp,均包括12个蛋白质编码基因、2个rRNA基因和22个tRNA基因,缺乏ATP8基因。羊仰口线虫编码蛋白质基因序列长10290bp,rRNA基因序列长1654bp,非编码区序列长324bp。整个线粒体基因组核苷酸组成为：A=27.8%,C=6.4%,G=17.0%,T=48.8%, A+T占76.5%,G+C占23.5%。牛仰口线虫蛋白质编码基因序列长10294bp,rRNA基因序列长1655bp,非编码区序列长346bp。整个线粒体基因组核苷酸组成为：A=26.8%,C=6.2%,G=16.9%,T=50.1%,A+T占76.9%,G+C占23.1%。两种虫体基因组碱基组成相似,明显偏好碱基A和T,整个基因组T的含量最高,而C的含量最低,这与其他钩口科线虫线粒体DNA中碱基分布相似。两种线虫的基因排列与圆线目的多数线虫相同,属GA7排列。以串联的线粒体12个蛋白质编码基因为基因标记,采用MP、BI和NJ法构建系统发生树的结果一致,无尾感器亚纲和有尾感器亚纲为两个大的分支,每个目的虫体各为一独立分支,在目的分支下,同科或同属虫体较近。在钩口科的这个进化类群中,仰口属为一分支,板口属和钩口属为另一分支,牛仰口线虫中国牦牛株与澳大利亚奶牛株关系最近,与十二指肠钩口线虫、犬钩口线虫和美洲板口线虫关系较羊仰口线虫远。这与利用ITS rDNA建树分析研究结果一致,说明线粒体全基因序列是研究寄生虫分子种系发生的良好基因标记。
本研究首次建立了鉴别牛仰口线虫和羊仰口线虫的PCR-RFLP方法,为其它近缘虫种或隐匿种的鉴别提供了参考；研究了不同宿主和不同地理来源羊仰口线虫线粒体部分基因序列的遗传多态性,证实羊仰口线虫种内变异较小,种间差异较大；获得了羊仰口线虫和牛仰口线虫中国牦牛株的线粒体全基因组序列并对其特征进行了分析,丰富了线虫线粒体基因组资料,基于线粒体基因组蛋白编码序列构建的系统发生树从分子水平上明确了羊仰口线虫、牛仰口线虫及其他线虫的进化关系,证明了线粒体全基因序列是研究寄生虫分子分类、遗传变异和系统发生的又一个良好基因标记。该项研究为其它钩虫和重要寄生虫系统发生学、群体遗传学和分子生态学的研究提供了基础资料。
Both Bunostomum phlebotomum and Bunostomum trigonocephalum, also known as hookworms, are blood-feeding nematodes which inhabit small intestines of cattle and sheep. Adult worms attach to the mucosa of the small intestine, suck blood, and may cause anemia, rapid weight loss and mandibular edema, as well as descent the performance trait and even death with heavy infection. Ancylostomiasis is endemic worldwide and causes serious hazard to animals, resulting in considerable economic losses to the live stock industries.
Previous studies showed strict host specificity for hookworms, which only infect definite hosts. However, recent studies found that some Bunostomum species can infect a variety of hosts. B. trigonocephalum not only infect sheep and goats, but also can infect cattle. This is also the case for B. phlebotomum. Therefore, it is difficult to identify these two hookworm species due to their similar morphological characters. The first part of my study was to establish a molecular method to identify B. phlebotomum and B. trigoncephalum, and to study phylogenetic relationships of these two species based on sequences of the internal transcribed spacer (ITS) ribosomal DNA (rDNA). The universal primers were designed based on published rDNA sequences of Ancylostomatidae nematodes. The total genomic DNA samples of these two species were individually extracted. The ITS rDNAs of B. phlebotomum and B. trigoncephalum were amplified, and sequenced from both sides. After analyzing restriction endonuclease sites in ITS rDNA seqeunces, the Nde I was chosen to identify the two hookworms. The ITS rDNA PCR amplicons of B. trigoncephalum were digested into two bands, while the amplicons of B. phlebotomum remain undigested. The established PCR method can effectively identify B. phlebotomum and B. trigoncephalum. Phylogenetic analyses based on the ITS sequences revealed that B. trigonocephalum and B. phlebotomum were closely related, but they represent two different species.
Due to maternal inheritance, high evolutionary rates and mutation rates, mitochondrial DNA (mtDNA) sequences provide useful markers for investigating population genetic structures, systematics and phylogenetics. The second part of my study was to examine genetic variations in four mitochondrial genes of B. trigoncephalum. A total of40samples were collected from four provinces (Heilongjiang, Yunnan, Jilin, Sichuan). Four partial mt genes, namely cytochrome c oxidase subunit1(pcoxl), NADH dehydrogenase subunit1(pnadl) and4(pnad4), and cytochrome b (pcytb) were amplified and sequenced. The intra-specific sequence variations of B. trigonocephalum were0-1.9%for pcoxl,0-1.6%for pnadl and0-1.7%for pnad5, and0-2.0%for pcytb. The nucleotide variation was related mainly to changes at the third codon position, while fewer changes were detected at the first or second codon position. The inter-specific variations among Ancylostoma caninum, Ancylostoma duodenale and Necator americanus were12.1-14.2%for pcoxl,17.6-19.4%for pnadl,16.0-21.6%for pnad5and13.7-16.0%for pcytb. These results demonstrated the existence of low-level intra-specific variation in mtDNA sequences among B. trigonocephalum isolates from different geographic regions.
The mitochondrial (mt) genomics represents an understudied but important field of molecular biology. Although there are many nematodes, only68complete or nearly complete mt genomes of nematodes have been sequenced. There is a paucity of information on mt genome dataset. The third part of my study was to determine sequences and structures of mt genomes of B. trigoncephalum and B. phlebotomum. PCR method was used to obtain complete mt genome sequences of B. trigoncephalum and B. phlebotomum. The phylogenetic trees were also re-constructed based on the protein-coding gene sequences of mt genomes to study the phylogenetic relationships between the B. trigoncephalum and B. phlebotomum. The complete mt genome sequences of B. trigoncephalum and B. phlebotomum were13771bp and13803bp, respectively. Both including12protein genes,2rRNA genes and22tRNA genes, lacking of ATP8gene. For B. trigoncephalum, the lengths of protein-coding gene, rRNA gene and non-coding sequence were10299bp,1654bp and324bp, respectively. The nucleotide compositions of the mt genome included27.8%,48.6%,17.0%and6.5%of A, T, G, C, and A+T contents of76.5%, and G+C of23.5%, respectively. For B. phlebotomum, the lengths of protein-coding gene, rRNA and non-coding sequences were10290bp,1655bp, and346bp, respectively. The nucleotide compositions of the mt genome included26.8%of A,50.1%of T,16.9%of G, and6.2%of C, with A+T contents of76.9%, G+C of23.1%. The mt genomes of B. trigoncephalum and B. phlebotomum were similar to prefer bases A and T, with highest for T, but lowest for C, which was consistent with other ancylostomatidae nematodes. The mt genes arrangements of two hookworms were consistent with most Strongylata nematodes and belonged to the GA7type. Phylogenetic relationships were reconstructed using the concatenated amino acid sequences of12protein-coding by three methods, namely MP, BI and NJ. The topological structures of trees were similar with different methods. Nematodes in classes Adenophorea and Secementia were located in two distinct clades, with parasites in each order clustered together. Within one order, nematodes in one Family and genus were closely related. Within the cluster of family Ancylostomatidae, the genus Bunostomum posited in one clade, and the genera Necator and Ancylostoma grouped in one clade. The B. phlebotomum isolated from Chinese yaks and that isolated from Australian dairy cattle were close related, compared with phylogenetic relationships with A. duodenale, A. caninum and N.r americanus. These results were consistent with that based on ITS rDNA, suggesting that the complete mt genome sequence was a reliable genetic marker for phylogenetic studies.
In conclusion, this study firstly established PCR-RFLP method to identify B. phlebotomum and B. trigoncephalum, which provided a reference for identification of other close-related or cryptic species. Based on partial mt DNA gene sequences, the genetic variations were examined among B. trigoncephalum isolated form different hosts and geographical origins. There were low intra-specific variations but significant inter-specific differences in these mt genes. The complete mt genome sequences were obtained for B. phlebotomum and B. trigoncephalum isolated from Chinese yaks. These findings enriched information of nematode mt genome dataset. Phylogenetic trees based on mt genome sequences clearly indicated genetic relationships of B. phlebotomum, B. trigoncephalum and other nematodes, suggesting that complete mt genome sequences will be another reliable genetic marker for molecular classification, genetic variation and phylogenetic studies. This thesis provides a foundation for studying the systematics, population gentics and ecology of other hookworms and parasites.
先前研究认为钩虫有很强的宿主特异性,一般情况下并不交叉传播。然而,随着研究的不断深入,研究人员发现有些种类的钩虫可以感染多种宿主,如羊仰口线虫主要寄生于绵羊和山羊,但也可感染牛；牛仰口线虫主要寄生于牛,有时也可感染羊。而两种仰口线虫形态十分相似,使得从形态学上准确鉴定虫种难度加大。鉴于此,本研究第一部分内容是在分子水平上建立一种鉴别牛仰口线虫和羊仰口线虫的方法,并以核糖体内转录间隔区(internal transcribed spacer, ITS)序列为基因标记探讨两种仰口线虫的亲缘关系。首先根据已发表的钩口科线虫核糖体DNA (rDNA)核苷酸序列,设计牛仰口线虫和羊仰口线虫rDNA ITS通用引物。分别提取牛仰口线虫和羊仰口线虫的基因组总DNA,进行PCR扩增和测序,获得两种仰口线虫的rDNA ITS序列,通过对ITS序列的酶切位点分析,选用限制性内切酶NdeⅠ对两种虫体的rDNA ITS PCR产物进行酶切,结果发现羊仰口线虫ITSrDNA序列被切成两段,而牛仰口线虫ITS rDNA序列则没有变化,成功建立了鉴别两种线虫的PCR-RFLP方法。该法简单、特异、而且需要DNA量较少,适合临床使用。利用rDNA ITS序列构建的系统发生树显示,牛仰口线虫和羊仰口线虫处于同一分支,亲缘关系较其它钩口科线虫近,但为两种不同的虫种。
由于线粒体DNA(mtDNA)具有进化速度快、基因突变率高、母性遗传等特点,是研究寄生虫系统发生学、群体遗传学和分子分类的理想分子标记。本研究的第二部分内容是研究不同宿主和不同地理来源羊仰口线虫线粒体部分基因序列的遗传多态性。对来自于黑龙江、云南、吉林、陕西四省绵羊和山羊的40条羊仰口线虫成虫样本的线粒体细胞色素c氧化酶亚基Ⅰ(cox1)基因、细胞色素b(cytb)基因、烟酰胺脱氢酶亚基Ⅰ(nad1)基因和亚基Ⅴ(nad5)基因的部分片段进行扩增,应用生物学软件对样本进行多态性分析,结果显示4段线粒体基因的种内变异情况分别为0.5%-1.6%(pcox1)、0.4%-1.7%(pcytb)、0.4%-1.2%(pnadl)和0.2%-1.9%(pnad5),在这4段线粒体部分基因序列中,核苷酸的变异位置大多发生在第三密码子位置,在第一密码子位置和第二密码子位置很少发生变异；与钩口科的犬钩口线虫、十二指肠钩口线虫和美洲板口线虫间的种间差异分别为12.1-14.2%(pcox1)、13.7-16.0%(pcytb)、17.6-19.4%(pnad1)和16.0-21.6%(pnad5),说明羊仰口线虫线粒体各段基因种内变异很小,但种间变异较大。
线粒体基因组学是研究不多但很重要的分子生物学领域。尽管线虫种类繁多,但目前关于线虫线粒体全基因组的研究却相对有限。截止目前,线粒体全基因组被完整或接近完整测序的线虫仅68种,线粒体全基因组的研究资料还相当欠缺。本研究第三部分内容是扩增羊仰口线虫和牛仰口线虫线粒体基因组,对整个基因组序列进行完整测序和序列分析,并基于线粒体基因组蛋白质编码基因序列构建系统发生树,阐明羊仰口线虫、牛仰口线虫与其他线虫的进化关系。本研究采用PCR方法获得的羊仰口线虫和牛仰口线虫线粒体全基因组序列分别为13771bp和13803bp,均包括12个蛋白质编码基因、2个rRNA基因和22个tRNA基因,缺乏ATP8基因。羊仰口线虫编码蛋白质基因序列长10290bp,rRNA基因序列长1654bp,非编码区序列长324bp。整个线粒体基因组核苷酸组成为：A=27.8%,C=6.4%,G=17.0%,T=48.8%, A+T占76.5%,G+C占23.5%。牛仰口线虫蛋白质编码基因序列长10294bp,rRNA基因序列长1655bp,非编码区序列长346bp。整个线粒体基因组核苷酸组成为：A=26.8%,C=6.2%,G=16.9%,T=50.1%,A+T占76.9%,G+C占23.1%。两种虫体基因组碱基组成相似,明显偏好碱基A和T,整个基因组T的含量最高,而C的含量最低,这与其他钩口科线虫线粒体DNA中碱基分布相似。两种线虫的基因排列与圆线目的多数线虫相同,属GA7排列。以串联的线粒体12个蛋白质编码基因为基因标记,采用MP、BI和NJ法构建系统发生树的结果一致,无尾感器亚纲和有尾感器亚纲为两个大的分支,每个目的虫体各为一独立分支,在目的分支下,同科或同属虫体较近。在钩口科的这个进化类群中,仰口属为一分支,板口属和钩口属为另一分支,牛仰口线虫中国牦牛株与澳大利亚奶牛株关系最近,与十二指肠钩口线虫、犬钩口线虫和美洲板口线虫关系较羊仰口线虫远。这与利用ITS rDNA建树分析研究结果一致,说明线粒体全基因序列是研究寄生虫分子种系发生的良好基因标记。
本研究首次建立了鉴别牛仰口线虫和羊仰口线虫的PCR-RFLP方法,为其它近缘虫种或隐匿种的鉴别提供了参考；研究了不同宿主和不同地理来源羊仰口线虫线粒体部分基因序列的遗传多态性,证实羊仰口线虫种内变异较小,种间差异较大；获得了羊仰口线虫和牛仰口线虫中国牦牛株的线粒体全基因组序列并对其特征进行了分析,丰富了线虫线粒体基因组资料,基于线粒体基因组蛋白编码序列构建的系统发生树从分子水平上明确了羊仰口线虫、牛仰口线虫及其他线虫的进化关系,证明了线粒体全基因序列是研究寄生虫分子分类、遗传变异和系统发生的又一个良好基因标记。该项研究为其它钩虫和重要寄生虫系统发生学、群体遗传学和分子生态学的研究提供了基础资料。
Both Bunostomum phlebotomum and Bunostomum trigonocephalum, also known as hookworms, are blood-feeding nematodes which inhabit small intestines of cattle and sheep. Adult worms attach to the mucosa of the small intestine, suck blood, and may cause anemia, rapid weight loss and mandibular edema, as well as descent the performance trait and even death with heavy infection. Ancylostomiasis is endemic worldwide and causes serious hazard to animals, resulting in considerable economic losses to the live stock industries.
Previous studies showed strict host specificity for hookworms, which only infect definite hosts. However, recent studies found that some Bunostomum species can infect a variety of hosts. B. trigonocephalum not only infect sheep and goats, but also can infect cattle. This is also the case for B. phlebotomum. Therefore, it is difficult to identify these two hookworm species due to their similar morphological characters. The first part of my study was to establish a molecular method to identify B. phlebotomum and B. trigoncephalum, and to study phylogenetic relationships of these two species based on sequences of the internal transcribed spacer (ITS) ribosomal DNA (rDNA). The universal primers were designed based on published rDNA sequences of Ancylostomatidae nematodes. The total genomic DNA samples of these two species were individually extracted. The ITS rDNAs of B. phlebotomum and B. trigoncephalum were amplified, and sequenced from both sides. After analyzing restriction endonuclease sites in ITS rDNA seqeunces, the Nde I was chosen to identify the two hookworms. The ITS rDNA PCR amplicons of B. trigoncephalum were digested into two bands, while the amplicons of B. phlebotomum remain undigested. The established PCR method can effectively identify B. phlebotomum and B. trigoncephalum. Phylogenetic analyses based on the ITS sequences revealed that B. trigonocephalum and B. phlebotomum were closely related, but they represent two different species.
Due to maternal inheritance, high evolutionary rates and mutation rates, mitochondrial DNA (mtDNA) sequences provide useful markers for investigating population genetic structures, systematics and phylogenetics. The second part of my study was to examine genetic variations in four mitochondrial genes of B. trigoncephalum. A total of40samples were collected from four provinces (Heilongjiang, Yunnan, Jilin, Sichuan). Four partial mt genes, namely cytochrome c oxidase subunit1(pcoxl), NADH dehydrogenase subunit1(pnadl) and4(pnad4), and cytochrome b (pcytb) were amplified and sequenced. The intra-specific sequence variations of B. trigonocephalum were0-1.9%for pcoxl,0-1.6%for pnadl and0-1.7%for pnad5, and0-2.0%for pcytb. The nucleotide variation was related mainly to changes at the third codon position, while fewer changes were detected at the first or second codon position. The inter-specific variations among Ancylostoma caninum, Ancylostoma duodenale and Necator americanus were12.1-14.2%for pcoxl,17.6-19.4%for pnadl,16.0-21.6%for pnad5and13.7-16.0%for pcytb. These results demonstrated the existence of low-level intra-specific variation in mtDNA sequences among B. trigonocephalum isolates from different geographic regions.
The mitochondrial (mt) genomics represents an understudied but important field of molecular biology. Although there are many nematodes, only68complete or nearly complete mt genomes of nematodes have been sequenced. There is a paucity of information on mt genome dataset. The third part of my study was to determine sequences and structures of mt genomes of B. trigoncephalum and B. phlebotomum. PCR method was used to obtain complete mt genome sequences of B. trigoncephalum and B. phlebotomum. The phylogenetic trees were also re-constructed based on the protein-coding gene sequences of mt genomes to study the phylogenetic relationships between the B. trigoncephalum and B. phlebotomum. The complete mt genome sequences of B. trigoncephalum and B. phlebotomum were13771bp and13803bp, respectively. Both including12protein genes,2rRNA genes and22tRNA genes, lacking of ATP8gene. For B. trigoncephalum, the lengths of protein-coding gene, rRNA gene and non-coding sequence were10299bp,1654bp and324bp, respectively. The nucleotide compositions of the mt genome included27.8%,48.6%,17.0%and6.5%of A, T, G, C, and A+T contents of76.5%, and G+C of23.5%, respectively. For B. phlebotomum, the lengths of protein-coding gene, rRNA and non-coding sequences were10290bp,1655bp, and346bp, respectively. The nucleotide compositions of the mt genome included26.8%of A,50.1%of T,16.9%of G, and6.2%of C, with A+T contents of76.9%, G+C of23.1%. The mt genomes of B. trigoncephalum and B. phlebotomum were similar to prefer bases A and T, with highest for T, but lowest for C, which was consistent with other ancylostomatidae nematodes. The mt genes arrangements of two hookworms were consistent with most Strongylata nematodes and belonged to the GA7type. Phylogenetic relationships were reconstructed using the concatenated amino acid sequences of12protein-coding by three methods, namely MP, BI and NJ. The topological structures of trees were similar with different methods. Nematodes in classes Adenophorea and Secementia were located in two distinct clades, with parasites in each order clustered together. Within one order, nematodes in one Family and genus were closely related. Within the cluster of family Ancylostomatidae, the genus Bunostomum posited in one clade, and the genera Necator and Ancylostoma grouped in one clade. The B. phlebotomum isolated from Chinese yaks and that isolated from Australian dairy cattle were close related, compared with phylogenetic relationships with A. duodenale, A. caninum and N.r americanus. These results were consistent with that based on ITS rDNA, suggesting that the complete mt genome sequence was a reliable genetic marker for phylogenetic studies.
In conclusion, this study firstly established PCR-RFLP method to identify B. phlebotomum and B. trigoncephalum, which provided a reference for identification of other close-related or cryptic species. Based on partial mt DNA gene sequences, the genetic variations were examined among B. trigoncephalum isolated form different hosts and geographical origins. There were low intra-specific variations but significant inter-specific differences in these mt genes. The complete mt genome sequences were obtained for B. phlebotomum and B. trigoncephalum isolated from Chinese yaks. These findings enriched information of nematode mt genome dataset. Phylogenetic trees based on mt genome sequences clearly indicated genetic relationships of B. phlebotomum, B. trigoncephalum and other nematodes, suggesting that complete mt genome sequences will be another reliable genetic marker for molecular classification, genetic variation and phylogenetic studies. This thesis provides a foundation for studying the systematics, population gentics and ecology of other hookworms and parasites.
引文
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