三种蝙蝠表观遗传多样性及其影响因素研究
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摘要
生物多样性面临着生境破碎化、过度开发利用以及全球气候变化等各方面的挑战，有机体不得不在进化过程中不断调整自己的表型，以应对各种环境变化。近期研究表明，除遗传因素外，表观遗传修饰在调节环境诱导表型过程中起到关键的作用，且这种变异的表观遗传信息可传递给后代，因而这种可遗传的表观遗传变异是自然种群中可遗传变异的重要源头，也是物种进化的重要动力之一。要评估表观遗传过程在生物表型形成以及调节有机体应对全球环境变化的作用，研究人员必须将生态学与表观遗传学有机结合起来，对自然生物种群开展表观遗传多样性调查及其影响因素的研究。
当前的表观遗传研究多数基于DNA甲基化展开的，其为目前研究最为透彻的表观遗传修饰，在许多生物过程中起到重要作用。植物自然种群已经进行许多相关研究，但动物自然种群仍缺乏大量的数据，真正意义上的动物种群表观遗传多样性研究仅限于虹鳟（Oncorhynchus mykiss）、红腹雅罗鱼（Chrosomus eos-neogaeus）和家麻雀（Passerdomesticus）3例，而关于野生哺乳动物种群表观遗传多样性研究则尚未开展。由于哺乳动物在生理特征上显著不同于其它动物，可能具有独特的应对环境变化的表观遗传机制，因而研究哺乳动物自然种群表观遗传多样性十分必要。蝙蝠具有种群数量大、分布广泛、生态功能显著以及对环境变化敏感等特征，可作为开展野生哺乳动物种群表观遗传遗传多样性研究的理想物种。
考虑到不同组织、不同发育阶段、不同冬眠行为状态下的DNA甲基化模式和水平并不相同，以及雌性的归家冲动行为，本论文提取了菲菊头蝠、大蹄蝠和亚种长翼蝠三种蝙蝠共131个雌性、成体、非冬眠样本的肌肉组织的基因组DNA，采用甲基化敏感扩增多态性技术（MSAP），每个物种各获得800余条片段。依据分类规则，将MSAP位点分成甲基化（MSP）和遗传位点（MIP），在此基础上，进行各个物种的甲基化水平和甲基化多态性的分析，判断种群间是否具有显著的DNA甲基化差异，以及探讨表观遗传多样性与遗传多样性、种群间地理距离以及气候、人为干扰程度、山洞大小、洞口隐蔽度和植被组成等环境变量之间存在的相关性。主要内容如下：
1.三种蝙蝠均具有较低的甲基化水平，其中菲菊头蝠为20.1-24.2%，大蹄蝠为20.4-26.5%，亚洲长翼蝠为20.6-22.0%。蝙蝠个体间存在高程度甲基化变异和低程度遗传变异，且三种蝙蝠的表观遗传多态性水平均显著高于相应的遗传多态性水平（香浓多样性指数），表明至少有一部分的表观遗传变异独立于遗传变异。植物种群的相关研究结果支持了这个结论，暗示蝙蝠种群这种高度种内表观遗传多样性可能广泛存在于野生哺乳动物种群，从而为物种应对自然环境变化提供更多选择。2.菲菊头蝠、大蹄蝠、亚洲长翼蝠种群分别有5.0%，30.7%和24.6%的甲基化位点，其频率在各物种种群间具有显著差异，表明蝙蝠种群间的表观遗传变异具有一定程度的分化。基于多位点开展的组间特征值分析表明，三种蝙蝠种群均存在显著的表观遗传结构，即表观遗传差异显著分成种群间和种群内，且主要变异存在于种群内，说明个体间存在大量DNA甲基化差异，这是表观遗传变异具备潜在进化作用的一个先决条件。
3.协惯量分析和Mantel检验（控制地理距离和环境变量）分别从个体水平和种群水平证实，三种蝙蝠种群间表观遗传多样性与相应的遗传多样性显著相关，表明蝙蝠种群的表观遗传多样性可能依赖于遗传多样性。然而，种群间较低的基因流和表观基因流表明，中性漂变也影响着蝙蝠种群表观遗传多样性水平。
4.顺序前进法分析结果表明，纬度显著影响菲菊头蝠表观遗传多样性（pseudo-F=2.162，P=0.044），并解释22.2%的种群间差异；年均湿度（pseudo-F=2.130，P=0.028）和洞口隐蔽度（pseudo-F=2.025，P=0.059）显著或弱显著贡献于大蹄蝠种群间的表观遗传多样性，能够解释42.8%的种群间差异；山洞附近植被类型（pseudo-F=3.128，P=0.014）、山洞大小（pseudo-F=2.000，P=0.023）、人为干扰程度（pseudo-F=1.932，P=0.094）等3个环境变量显著或弱显著影响亚洲长翼蝠表观遗传多样性，能解释68.3%的种群间变异。分析结果表明，环境变量影响蝙蝠种群表观遗传多样性，表观遗传变异是蝙蝠应对环境变化的另一途径，蝙蝠可以通过调整DNA甲基化水平来适应新环境。
蝙蝠种群具有高水平的表观遗传变异，主要受其遗传多样性、中性漂变以及环境诱导等方面共同影响。蝙蝠可以通过表观遗传变异提高对环境变化的耐受性，有利于蝙蝠物种的进化。然而，当前人类活动带来的快速全球气候变化、生境破碎化的影响超过蝙蝠的适应能力，导致蝙蝠种群数量锐减，因而人类仍应尽量减少对蝙蝠种群的干扰。
Biodiversity faces challenges from habitat fragmentation, over exploitation, and globalclimate change. Organisms have to adjust their phenotype in responding to variousenvironmental stresses. Recent studies showed that epigenetic modifications have animportant role in mediating environmentally induced phenotypic variation, and thoseepigenetic variances could be inherited by future generations. Therefore, epigenetic processesare considered as another source of the natural heritable variation, and another dimension inevolution. Crucial steps before estimating the potential role of epigenetic variation inproducing new phenotypes and responding to global environmental change for organisms,are exploring the genomic epigenetic diversity in natural populations and finding itsinfluencing factors.
DNA methylation is one of the best studied epigenetic mechanisms, and has a criticalrole in many key biological processes. Till now, related researches have been done in wildplant populations; however, limited data are explored in wild animals, and only3studiesabout population epigenetic diversity were reported on steelhead (Oncorhynchus mykiss),redbelly dac (Chrosomus eos-neogaeus), and house sparrows (Passer domesticus). Thereis no study about population epigenetic has been done on wild mammal populationsyet, while mammals have special evolution mechanisms to adapt to varied environments,and they may have different epigenetic processes in responding to environmental variationscomparing with other animals. Thus, it’s necessary to explore the population epigeneticdiversity of wild mammals. Bats have large populations, wide distributions, significantecological functions, and are sensitive to environmental variance; therefore, they may presentan opportunity to explore epigenetic variance in natural mammalian populations.
Considering that there exist difference of DNA methyaltion among different tissues,developments, and behaviors, we extracted genomic DNA from muscle tissues of131female,adult and non-hibernate individuals in3bat species: Rhinolophus pusillus, Hipposiderosarmiger, and Miniopterus fuliginosus. Using methylation-sensitive amplified polymorphism(MSAP) technique, we obtained more than800bands in each species to explore thesequestions in bat populations: what’s the level and polymorphism of genome-wide DNAmethylation, whether DNA methylation diversity is significant structured into distinctbetween-and within-population components and whether it is significant correlated withgenetic diversity, geographic distance, and environmental factors, e.g. coordinates, climatefactors, human disturbance, roosting size, concealed degree and plant types. The maincontexts were as follows:
1. The methylation levels in3bats were,20.1-24.2%in R. pusillus,20.4-26.5%in H.armiger, and20.6-22.0%in M. fuliginosus. There existed extensive methylation variationbut low level in genetic variation in those bat populations, and epigenetic diversity exceeded conventional genetic diversity when the two magnitudes are compared using the Shannonindex, implying that at least partly epigenetic variance is dependent from genetic variance.Similar results were found in wild plant populations, implied that extensive intraspecificepigenetic variation found in our study is probably widespread in wild populations, andsupports an alternative system for organism in responding to natural variation.
2. There were about5.0%,30.7%and24.6%methylated loci were significantdifferentiation among populations in R. pusillus, H. armiger, and M. fuliginosus, respectively,indicating estensive epigenetic differentiation among populations in each species.Between-group eigen analyses (BGEA) showed significant epigenetic structure existing ineach bats based on multilocus epigenetic population differentiation, i.e. methylation-basedepigenetic variation was structured into distinct between-and within-population components,implying extensive individual epigenotypic variation, which is a critical prerequisite forepigenetic variation to have some microevolutionary potential.
3. Both co-inertia analysis and Mantel tests (controlling geographic distance andenvironmental variables) showed that epigenetic variance was significant correlated withgenetic profile in those3bats, implying epigenetic variance is dependent to genetic variation.However, low genetic flow and epigenetic flow among populations implied that neutral driftcould also result in epigenetic variations.
4. Sequential forward selection analysis showed that latitude (pseudo-F=2.162, P=0.044) had signifiant effects on epigenetic diversity among R. pusillus populations andaccounted for22.2%variance; mean annual humidity (pseudo-F=2.130, P=0.028) andconcealed degree of caves (pseudo-F=2.025，P=0.059) had marginally significant effectson epigenetic difference between H. armiger populations and accounted for42.8%variance;plant types(pseudo-F=3.128，P=0.014), roosting size (pseudo-F=2.000，P=0.023), andhuman disturbance (pseudo-F=1.932，P=0.094) had significant or marginally significanteffects on population epigenetic difference, accounting altogether for68.3%variance. Aboveresults indicated that environmental factors had significant effects on epigenetic diversity infemale bats populations. Therefore, epigenetic mechanism is an alternative system for bats toresponse to environmental variance, or bats could adapt to new environment via DNAmethylation variance.
The bat populations have high level epigenetic diversities, which were affected bycorresponding genetic diversity, neutral drift, and environmental changes. It’s beneficial forbat species in improving their tolerance by epigenetic mechanisms in evolution, however, thepopulation size of bats are reduced by negative effects from global climate change, andhabitat destruction, which are induced by human activities. Thus, we still need to reducenegative disturbances to bats.
当前的表观遗传研究多数基于DNA甲基化展开的，其为目前研究最为透彻的表观遗传修饰，在许多生物过程中起到重要作用。植物自然种群已经进行许多相关研究，但动物自然种群仍缺乏大量的数据，真正意义上的动物种群表观遗传多样性研究仅限于虹鳟（Oncorhynchus mykiss）、红腹雅罗鱼（Chrosomus eos-neogaeus）和家麻雀（Passerdomesticus）3例，而关于野生哺乳动物种群表观遗传多样性研究则尚未开展。由于哺乳动物在生理特征上显著不同于其它动物，可能具有独特的应对环境变化的表观遗传机制，因而研究哺乳动物自然种群表观遗传多样性十分必要。蝙蝠具有种群数量大、分布广泛、生态功能显著以及对环境变化敏感等特征，可作为开展野生哺乳动物种群表观遗传遗传多样性研究的理想物种。
考虑到不同组织、不同发育阶段、不同冬眠行为状态下的DNA甲基化模式和水平并不相同，以及雌性的归家冲动行为，本论文提取了菲菊头蝠、大蹄蝠和亚种长翼蝠三种蝙蝠共131个雌性、成体、非冬眠样本的肌肉组织的基因组DNA，采用甲基化敏感扩增多态性技术（MSAP），每个物种各获得800余条片段。依据分类规则，将MSAP位点分成甲基化（MSP）和遗传位点（MIP），在此基础上，进行各个物种的甲基化水平和甲基化多态性的分析，判断种群间是否具有显著的DNA甲基化差异，以及探讨表观遗传多样性与遗传多样性、种群间地理距离以及气候、人为干扰程度、山洞大小、洞口隐蔽度和植被组成等环境变量之间存在的相关性。主要内容如下：
1.三种蝙蝠均具有较低的甲基化水平，其中菲菊头蝠为20.1-24.2%，大蹄蝠为20.4-26.5%，亚洲长翼蝠为20.6-22.0%。蝙蝠个体间存在高程度甲基化变异和低程度遗传变异，且三种蝙蝠的表观遗传多态性水平均显著高于相应的遗传多态性水平（香浓多样性指数），表明至少有一部分的表观遗传变异独立于遗传变异。植物种群的相关研究结果支持了这个结论，暗示蝙蝠种群这种高度种内表观遗传多样性可能广泛存在于野生哺乳动物种群，从而为物种应对自然环境变化提供更多选择。2.菲菊头蝠、大蹄蝠、亚洲长翼蝠种群分别有5.0%，30.7%和24.6%的甲基化位点，其频率在各物种种群间具有显著差异，表明蝙蝠种群间的表观遗传变异具有一定程度的分化。基于多位点开展的组间特征值分析表明，三种蝙蝠种群均存在显著的表观遗传结构，即表观遗传差异显著分成种群间和种群内，且主要变异存在于种群内，说明个体间存在大量DNA甲基化差异，这是表观遗传变异具备潜在进化作用的一个先决条件。
3.协惯量分析和Mantel检验（控制地理距离和环境变量）分别从个体水平和种群水平证实，三种蝙蝠种群间表观遗传多样性与相应的遗传多样性显著相关，表明蝙蝠种群的表观遗传多样性可能依赖于遗传多样性。然而，种群间较低的基因流和表观基因流表明，中性漂变也影响着蝙蝠种群表观遗传多样性水平。
4.顺序前进法分析结果表明，纬度显著影响菲菊头蝠表观遗传多样性（pseudo-F=2.162，P=0.044），并解释22.2%的种群间差异；年均湿度（pseudo-F=2.130，P=0.028）和洞口隐蔽度（pseudo-F=2.025，P=0.059）显著或弱显著贡献于大蹄蝠种群间的表观遗传多样性，能够解释42.8%的种群间差异；山洞附近植被类型（pseudo-F=3.128，P=0.014）、山洞大小（pseudo-F=2.000，P=0.023）、人为干扰程度（pseudo-F=1.932，P=0.094）等3个环境变量显著或弱显著影响亚洲长翼蝠表观遗传多样性，能解释68.3%的种群间变异。分析结果表明，环境变量影响蝙蝠种群表观遗传多样性，表观遗传变异是蝙蝠应对环境变化的另一途径，蝙蝠可以通过调整DNA甲基化水平来适应新环境。
蝙蝠种群具有高水平的表观遗传变异，主要受其遗传多样性、中性漂变以及环境诱导等方面共同影响。蝙蝠可以通过表观遗传变异提高对环境变化的耐受性，有利于蝙蝠物种的进化。然而，当前人类活动带来的快速全球气候变化、生境破碎化的影响超过蝙蝠的适应能力，导致蝙蝠种群数量锐减，因而人类仍应尽量减少对蝙蝠种群的干扰。
Biodiversity faces challenges from habitat fragmentation, over exploitation, and globalclimate change. Organisms have to adjust their phenotype in responding to variousenvironmental stresses. Recent studies showed that epigenetic modifications have animportant role in mediating environmentally induced phenotypic variation, and thoseepigenetic variances could be inherited by future generations. Therefore, epigenetic processesare considered as another source of the natural heritable variation, and another dimension inevolution. Crucial steps before estimating the potential role of epigenetic variation inproducing new phenotypes and responding to global environmental change for organisms,are exploring the genomic epigenetic diversity in natural populations and finding itsinfluencing factors.
DNA methylation is one of the best studied epigenetic mechanisms, and has a criticalrole in many key biological processes. Till now, related researches have been done in wildplant populations; however, limited data are explored in wild animals, and only3studiesabout population epigenetic diversity were reported on steelhead (Oncorhynchus mykiss),redbelly dac (Chrosomus eos-neogaeus), and house sparrows (Passer domesticus). Thereis no study about population epigenetic has been done on wild mammal populationsyet, while mammals have special evolution mechanisms to adapt to varied environments,and they may have different epigenetic processes in responding to environmental variationscomparing with other animals. Thus, it’s necessary to explore the population epigeneticdiversity of wild mammals. Bats have large populations, wide distributions, significantecological functions, and are sensitive to environmental variance; therefore, they may presentan opportunity to explore epigenetic variance in natural mammalian populations.
Considering that there exist difference of DNA methyaltion among different tissues,developments, and behaviors, we extracted genomic DNA from muscle tissues of131female,adult and non-hibernate individuals in3bat species: Rhinolophus pusillus, Hipposiderosarmiger, and Miniopterus fuliginosus. Using methylation-sensitive amplified polymorphism(MSAP) technique, we obtained more than800bands in each species to explore thesequestions in bat populations: what’s the level and polymorphism of genome-wide DNAmethylation, whether DNA methylation diversity is significant structured into distinctbetween-and within-population components and whether it is significant correlated withgenetic diversity, geographic distance, and environmental factors, e.g. coordinates, climatefactors, human disturbance, roosting size, concealed degree and plant types. The maincontexts were as follows:
1. The methylation levels in3bats were,20.1-24.2%in R. pusillus,20.4-26.5%in H.armiger, and20.6-22.0%in M. fuliginosus. There existed extensive methylation variationbut low level in genetic variation in those bat populations, and epigenetic diversity exceeded conventional genetic diversity when the two magnitudes are compared using the Shannonindex, implying that at least partly epigenetic variance is dependent from genetic variance.Similar results were found in wild plant populations, implied that extensive intraspecificepigenetic variation found in our study is probably widespread in wild populations, andsupports an alternative system for organism in responding to natural variation.
2. There were about5.0%,30.7%and24.6%methylated loci were significantdifferentiation among populations in R. pusillus, H. armiger, and M. fuliginosus, respectively,indicating estensive epigenetic differentiation among populations in each species.Between-group eigen analyses (BGEA) showed significant epigenetic structure existing ineach bats based on multilocus epigenetic population differentiation, i.e. methylation-basedepigenetic variation was structured into distinct between-and within-population components,implying extensive individual epigenotypic variation, which is a critical prerequisite forepigenetic variation to have some microevolutionary potential.
3. Both co-inertia analysis and Mantel tests (controlling geographic distance andenvironmental variables) showed that epigenetic variance was significant correlated withgenetic profile in those3bats, implying epigenetic variance is dependent to genetic variation.However, low genetic flow and epigenetic flow among populations implied that neutral driftcould also result in epigenetic variations.
4. Sequential forward selection analysis showed that latitude (pseudo-F=2.162, P=0.044) had signifiant effects on epigenetic diversity among R. pusillus populations andaccounted for22.2%variance; mean annual humidity (pseudo-F=2.130, P=0.028) andconcealed degree of caves (pseudo-F=2.025，P=0.059) had marginally significant effectson epigenetic difference between H. armiger populations and accounted for42.8%variance;plant types(pseudo-F=3.128，P=0.014), roosting size (pseudo-F=2.000，P=0.023), andhuman disturbance (pseudo-F=1.932，P=0.094) had significant or marginally significanteffects on population epigenetic difference, accounting altogether for68.3%variance. Aboveresults indicated that environmental factors had significant effects on epigenetic diversity infemale bats populations. Therefore, epigenetic mechanism is an alternative system for bats toresponse to environmental variance, or bats could adapt to new environment via DNAmethylation variance.
The bat populations have high level epigenetic diversities, which were affected bycorresponding genetic diversity, neutral drift, and environmental changes. It’s beneficial forbat species in improving their tolerance by epigenetic mechanisms in evolution, however, thepopulation size of bats are reduced by negative effects from global climate change, andhabitat destruction, which are induced by human activities. Thus, we still need to reducenegative disturbances to bats.
引文
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