薜荔（Ficus pumila）及其传粉小蜂（Wiebesia spp.）的分化与比较亲缘地理学
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摘要
植物与昆虫间的协同进化被认为是植食性昆虫多样性形成的重要原因,往往导致昆虫与其宿主植物的协同成种；两者系统进化树的不一致又暗示着协同成种不是唯一的机制,宿主转移等其他因素在植食性昆虫的分化成种中也起着非常重要的作用。除了与植物的相互作用,近年来的研究显示地质历史事件也是十分关键的因素,山脉的隆起、沟壑的形成造成种群间隔离,于是缺乏交流的种群逐渐分化；气候波动引起物种分布范围的收缩或扩张,对物种分布格局和遗传结构的塑造有重要作用。
榕和榕小蜂是专一性最强的共生体系之一,早期研究认为它们是“一对一”的关系,近年来通过分子标记揭示出越来越多“一对多”,甚至“多对一”的现象。尽管宿主转移是可能的解释,但协同成种是榕与传粉小蜂演化的重要模式,意味着更多的情况是同一宿主成种,地质历史事件在小蜂的分化中有着不可忽视的作用。薜荔为雌雄异株榕,在我国长江以南地区广泛分布,依靠专一性的传粉小蜂为其授粉。本论文以薜荔和薜荔传粉小蜂为研究对象,通过分子标记对薜荔分布区范围内薜荔传粉小蜂的种类进行鉴定,确定薜荔小蜂隐存种的分布格局,并对它们遗传结构及扩散格局进行分析,推断地质历史事件在其分化中的作用。气候波动造成物种分布范围的改变,分化的隐存种再次接触,由于对相同资源的利用,它们必定存在分化,小蜂短暂的出飞期是关键,因此对舟山岛屿地区两个隐存种的物候分化做了研究。另外,对比研究薜荔和薜荔小蜂的遗传结构及种群动态,并结合薜荔的生态位模型分析,推测地质历史事件对它们的影响。主要得出以下结论：
1)在我国薜荔分布范围内存在3个薜荔传粉小蜂隐存种,分别为Wiebesiaspp.1,2和3。它们主要呈异域分布：南岭、武夷山脉以及延伸至浙江境内的仙霞岭和天台山脉是物种1和2的主要分界线,交界的一些种群中存在2个物种共存的现象；物种3主要分布在舟山群岛,大部分与物种1同域,另外在大陆宁德(ND)种群中也有分布,台湾地区的爱玉子传粉小蜂也为物种3。
薜荔小蜂3个物种的分化时间、种群遗传结构以及扩散格局揭示出地质历史事件是造成它们隔离分化的原因。第四纪冰期以及间冰期波动的气候导致3个物种分布范围的收缩与扩张,从而形成今天的分布格局。
2)薜荔与薜荔小蜂的物候高度匹配,薜荔雄株一年存在2-3次花期,以春季和夏季为主,相应的薜荔小蜂一年有2-3个世代。同域分布的薜荔小蜂物种1和物种3存在物候分化,表现在物种1早于物种3出飞。
尽管它们可以同株共存,但在出飞时间上仍然表现出差异,同果共存的现象很少,仅发现一例。被一个物种占据的薜荔很难再被另一个物种所用,暗示着小蜂的物候会诱导薜荔物候发生变化,但具体机制尚待研究。
3)薜荔和薜荔小蜂虽为强制性互利共生体系,经历共同的地质历史事件。小蜂的扩散影响薜荔的花粉流,但两者的遗传格局却非常不一致。尽管拥有相同的冰期避难所,但它们不同的生活史特征导致扩散能力的明显差异是造成这种不一致格局的主要原因。
种群遗传结构及种群动态分析揭示出薜荔和薜荔小蜂存在多个冰期避难所,且二者的冰期后扩散路线不一致。
小蜂物种1的两个潜在避难所为南岭以北的湖南境内,以及武夷山南段西侧地区。冰期后南岭以北的种群受地形限制并未扩至湖南以外,而武夷山西侧的种群则往北以及沿着武夷山脉、浙江仙霞岭一带扩往浙江境内,并且扩散至舟山岛屿上。
物种2在南部的沿海地区存在一个冰期避难所；西部种群有较高的遗传多样性,因此这一带也是潜在的冰期避难所；海南岛小蜂线粒体COI单倍型与大陆分化较大,隔离是分化的重要因素,因此推测冰期时这里也是潜在的避难所；另外台湾也是潜在的避难所。
岛屿是物种3的潜在冰期避难所。台湾爱玉子的传粉小蜂为物种3,结合爱玉子与薜荔之间的分化,推测台湾是物种3的形成地,因此也是冰期避难所；另外,如果物种3在末次盛冰期以前就扩至舟山岛屿地区,那这一地区也是其潜在的冰期避难所。
小蜂的避难所即是薜荔的避难所,只是冰期后薜荔呈现出与小蜂不同的扩散路线。
Coevolution was thought as an important factor to promote diversity of herbivorous insects. However, incongruence topology of phylogenetic trees between insects and their host plants were frequently observed in recent studies, suggesting that cospeciation was not the sole mechanism, and other factors such as host shift, also played an critical role in the diversification of insects. In addition, geological events also contributed to the diversification of insects. Uplifts of mountains and formation of straits or rivers led to the isolation and divergence of populations. And climatic fluctuations drove the range shifts of species, resulting in the changing of population genetic structure.
Fig trees and their pollinating wasps constitute perhaps the most obligate mutualisms in nature, providing ideal systems to understand the role of geological evens in insects' speication and in shaping genetic structure of host plants and insects. Previous observations suggested that a fig tree is pollinated by a specific pollinating wasp, i.e.,"one-to-one" rule. However, recent studies using molecular markers found increasing number of exceptions, indicating that "one fig-to-multiple fig wasps" or "multiple figs-to-one fig wasp" may be more common. The interaction between Ficus pumila and its pollinating wasps(Wiebesia spp.) is one of these exceptions. Ficus pumila is pollinated by three cryptic wasp species, which are sister species, hinting that they diverged in one host species.
To explore how geological events shape the divergence of F. pumila and Wiebesia spp., we used molecular makers to study the distribution pattern of these cryptic pollinators and to decipher their genetic structures. And we also studied their genetic responses to geological events by comparing phylogeographical patterns of the two intimately interacting partners. Two cryptic pollinators coexist in Zhoushan Archipelago. To understand the way of their coexistence, we observed their emergence phenologies. Finally, we got following conclusions.
1) There are three cryptic pollinators in our study range, i.e., Wiebesia spp.1,2and3. They are mainly distributing in allopatry. Mountains are main boundaries of Wiebesia spp.1and2. Wiebesia sp.3is mainly located in Zhoushan Archipelago, where it is in sympatric with Wiebesia sp.1, and it was also found in a mainland population, i.e., Ningde. Besides, in Taiwan, Wiebesia sp.3is the sole pollinator of F. pumila var. awkeotsang. This study also confirmed that the formation of Taiwan Strait and the uplift of Wuyi Mountain were the key factors of divergence and speciation of the F. pumila and its pollinating wasps.
2) We observed two or three crops per year for male F. pumila, corresponding with two or three generations per year of the pollinators. In Zhoushan Archipelago, where two species coexist, we found that Wiebesia sp.1emerged earlier than Wiebesia sp.3. They could coexist in one plant, but diverged in phenology. We found only one case that a fig synconium contained both fig wasps. Fig plants were usually occupied by the same pollinating wasp in different years, hinting that the phenology of E pumila was induced by the pollinators. However further studies are needed.
3) Due to their obligate dependence on each other, F. pumila and Wiebesia spp. were affected by the same geological events. However, their genetic structures were quite different, a results of different dispersal abilities.
According to their population genetic structures and population demographics, we inferred multiple refugia and different postglacial dispersal rutes for F. pumila and Wiebesia spp. Wiebesia sp.1had two potential glacial refugia, located at the northern part of Nanling Mountains in Hunan province, and the west of Wuyi Mountain. Postglacial recolonization from the first refugium was limited in Hunan province by topography. While populations in the second refugium expanded along Wuyi Mountain and Xianxia Mountains, and also to island habitats.
There were several potential refugia of Wiebesia sp.2. A refugium was located in south coast of China. High genetic diversity in west populations indicated this place was also a potential refugium. The high genetic divergence between wasps in Hainan Island and the other mainland populations provided evidence for Hainan or nearby place as a glacial refugium. In addition, Taiwan was also a refugium.
Islands were the potential refugia of Wiebesia sp.3. Taiwan was one of the palces as a shelter for Wiebesia sp.3in glacial period, because Wiebesia sp.3is the pollinator of F.pumila. var. awkeotsang. Meanwhile, if Wiebesia sp.3had dispersed to the islands of northern part before LGM, then this place was another potential refugium.
F. pumila had the same refugia as Wiebesia spp., but showed different dispersal routes. Populations in east of Wuyi Mountain were originated from the south coast refugium, and complicated dispersal patterns in west populations were shaped by the topography.
榕和榕小蜂是专一性最强的共生体系之一,早期研究认为它们是“一对一”的关系,近年来通过分子标记揭示出越来越多“一对多”,甚至“多对一”的现象。尽管宿主转移是可能的解释,但协同成种是榕与传粉小蜂演化的重要模式,意味着更多的情况是同一宿主成种,地质历史事件在小蜂的分化中有着不可忽视的作用。薜荔为雌雄异株榕,在我国长江以南地区广泛分布,依靠专一性的传粉小蜂为其授粉。本论文以薜荔和薜荔传粉小蜂为研究对象,通过分子标记对薜荔分布区范围内薜荔传粉小蜂的种类进行鉴定,确定薜荔小蜂隐存种的分布格局,并对它们遗传结构及扩散格局进行分析,推断地质历史事件在其分化中的作用。气候波动造成物种分布范围的改变,分化的隐存种再次接触,由于对相同资源的利用,它们必定存在分化,小蜂短暂的出飞期是关键,因此对舟山岛屿地区两个隐存种的物候分化做了研究。另外,对比研究薜荔和薜荔小蜂的遗传结构及种群动态,并结合薜荔的生态位模型分析,推测地质历史事件对它们的影响。主要得出以下结论：
1)在我国薜荔分布范围内存在3个薜荔传粉小蜂隐存种,分别为Wiebesiaspp.1,2和3。它们主要呈异域分布：南岭、武夷山脉以及延伸至浙江境内的仙霞岭和天台山脉是物种1和2的主要分界线,交界的一些种群中存在2个物种共存的现象；物种3主要分布在舟山群岛,大部分与物种1同域,另外在大陆宁德(ND)种群中也有分布,台湾地区的爱玉子传粉小蜂也为物种3。
薜荔小蜂3个物种的分化时间、种群遗传结构以及扩散格局揭示出地质历史事件是造成它们隔离分化的原因。第四纪冰期以及间冰期波动的气候导致3个物种分布范围的收缩与扩张,从而形成今天的分布格局。
2)薜荔与薜荔小蜂的物候高度匹配,薜荔雄株一年存在2-3次花期,以春季和夏季为主,相应的薜荔小蜂一年有2-3个世代。同域分布的薜荔小蜂物种1和物种3存在物候分化,表现在物种1早于物种3出飞。
尽管它们可以同株共存,但在出飞时间上仍然表现出差异,同果共存的现象很少,仅发现一例。被一个物种占据的薜荔很难再被另一个物种所用,暗示着小蜂的物候会诱导薜荔物候发生变化,但具体机制尚待研究。
3)薜荔和薜荔小蜂虽为强制性互利共生体系,经历共同的地质历史事件。小蜂的扩散影响薜荔的花粉流,但两者的遗传格局却非常不一致。尽管拥有相同的冰期避难所,但它们不同的生活史特征导致扩散能力的明显差异是造成这种不一致格局的主要原因。
种群遗传结构及种群动态分析揭示出薜荔和薜荔小蜂存在多个冰期避难所,且二者的冰期后扩散路线不一致。
小蜂物种1的两个潜在避难所为南岭以北的湖南境内,以及武夷山南段西侧地区。冰期后南岭以北的种群受地形限制并未扩至湖南以外,而武夷山西侧的种群则往北以及沿着武夷山脉、浙江仙霞岭一带扩往浙江境内,并且扩散至舟山岛屿上。
物种2在南部的沿海地区存在一个冰期避难所；西部种群有较高的遗传多样性,因此这一带也是潜在的冰期避难所；海南岛小蜂线粒体COI单倍型与大陆分化较大,隔离是分化的重要因素,因此推测冰期时这里也是潜在的避难所；另外台湾也是潜在的避难所。
岛屿是物种3的潜在冰期避难所。台湾爱玉子的传粉小蜂为物种3,结合爱玉子与薜荔之间的分化,推测台湾是物种3的形成地,因此也是冰期避难所；另外,如果物种3在末次盛冰期以前就扩至舟山岛屿地区,那这一地区也是其潜在的冰期避难所。
小蜂的避难所即是薜荔的避难所,只是冰期后薜荔呈现出与小蜂不同的扩散路线。
Coevolution was thought as an important factor to promote diversity of herbivorous insects. However, incongruence topology of phylogenetic trees between insects and their host plants were frequently observed in recent studies, suggesting that cospeciation was not the sole mechanism, and other factors such as host shift, also played an critical role in the diversification of insects. In addition, geological events also contributed to the diversification of insects. Uplifts of mountains and formation of straits or rivers led to the isolation and divergence of populations. And climatic fluctuations drove the range shifts of species, resulting in the changing of population genetic structure.
Fig trees and their pollinating wasps constitute perhaps the most obligate mutualisms in nature, providing ideal systems to understand the role of geological evens in insects' speication and in shaping genetic structure of host plants and insects. Previous observations suggested that a fig tree is pollinated by a specific pollinating wasp, i.e.,"one-to-one" rule. However, recent studies using molecular markers found increasing number of exceptions, indicating that "one fig-to-multiple fig wasps" or "multiple figs-to-one fig wasp" may be more common. The interaction between Ficus pumila and its pollinating wasps(Wiebesia spp.) is one of these exceptions. Ficus pumila is pollinated by three cryptic wasp species, which are sister species, hinting that they diverged in one host species.
To explore how geological events shape the divergence of F. pumila and Wiebesia spp., we used molecular makers to study the distribution pattern of these cryptic pollinators and to decipher their genetic structures. And we also studied their genetic responses to geological events by comparing phylogeographical patterns of the two intimately interacting partners. Two cryptic pollinators coexist in Zhoushan Archipelago. To understand the way of their coexistence, we observed their emergence phenologies. Finally, we got following conclusions.
1) There are three cryptic pollinators in our study range, i.e., Wiebesia spp.1,2and3. They are mainly distributing in allopatry. Mountains are main boundaries of Wiebesia spp.1and2. Wiebesia sp.3is mainly located in Zhoushan Archipelago, where it is in sympatric with Wiebesia sp.1, and it was also found in a mainland population, i.e., Ningde. Besides, in Taiwan, Wiebesia sp.3is the sole pollinator of F. pumila var. awkeotsang. This study also confirmed that the formation of Taiwan Strait and the uplift of Wuyi Mountain were the key factors of divergence and speciation of the F. pumila and its pollinating wasps.
2) We observed two or three crops per year for male F. pumila, corresponding with two or three generations per year of the pollinators. In Zhoushan Archipelago, where two species coexist, we found that Wiebesia sp.1emerged earlier than Wiebesia sp.3. They could coexist in one plant, but diverged in phenology. We found only one case that a fig synconium contained both fig wasps. Fig plants were usually occupied by the same pollinating wasp in different years, hinting that the phenology of E pumila was induced by the pollinators. However further studies are needed.
3) Due to their obligate dependence on each other, F. pumila and Wiebesia spp. were affected by the same geological events. However, their genetic structures were quite different, a results of different dispersal abilities.
According to their population genetic structures and population demographics, we inferred multiple refugia and different postglacial dispersal rutes for F. pumila and Wiebesia spp. Wiebesia sp.1had two potential glacial refugia, located at the northern part of Nanling Mountains in Hunan province, and the west of Wuyi Mountain. Postglacial recolonization from the first refugium was limited in Hunan province by topography. While populations in the second refugium expanded along Wuyi Mountain and Xianxia Mountains, and also to island habitats.
There were several potential refugia of Wiebesia sp.2. A refugium was located in south coast of China. High genetic diversity in west populations indicated this place was also a potential refugium. The high genetic divergence between wasps in Hainan Island and the other mainland populations provided evidence for Hainan or nearby place as a glacial refugium. In addition, Taiwan was also a refugium.
Islands were the potential refugia of Wiebesia sp.3. Taiwan was one of the palces as a shelter for Wiebesia sp.3in glacial period, because Wiebesia sp.3is the pollinator of F.pumila. var. awkeotsang. Meanwhile, if Wiebesia sp.3had dispersed to the islands of northern part before LGM, then this place was another potential refugium.
F. pumila had the same refugia as Wiebesia spp., but showed different dispersal routes. Populations in east of Wuyi Mountain were originated from the south coast refugium, and complicated dispersal patterns in west populations were shaped by the topography.
引文
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