枯叶蛱蝶生物学特征及种内分化的分子遗传研究
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摘要
枯叶蛱蝶Kallima inachus (Doyére, 1840),属鳞翅目Lepidoptera,蛱蝶科Nymphalidae,蛱蝶亚科Nymphalinae,斑蛱蝶族Hypolimn(i枯叶蛱蝶族Kallimini),枯叶蛱蝶属Kallima Doubleday。世界著名的拟态蝴蝶,具有很高的经济、文化和科学研究价值。前人主要按照分布区划分了6个亚种,目前对其生物学生态学特性了解不多。由于生境丧失或退化,许多地方的种群正在迅速下降。
研究表明,在四川峨眉,枯叶蛱蝶实验种群一年发生3代,以第1和第2代为主,以滞育成虫越冬。第1代雌成虫和8月中旬前羽化的第2代雌成虫的大部分个体参与当年繁殖,少部分进入生殖滞育。第3代雌成虫和8月中旬后羽化的第2代雌成虫的绝大多数进入生殖滞育。最后,三个世代中的滞育个体汇聚成越冬成虫群体。成虫的羽化、取食、求偶、交配和产卵等活动都在白天进行,且与阳光和气温有密切关系。在野外,成虫的主要补充营养为自阔叶树树干虫蛀伤口中流出的树液和半腐烂的水果,有时也汲食动物粪尿。实验条件下,成虫汲食新鲜果汁、发酵水果、蜂糖水溶液、动物粪便和尿液等。雄成虫的求偶行为属于典型的“等候型”,在求偶时段有强烈的领域性。在不遭受天敌捕食的条件下,繁殖雌成虫的平均寿命为36.67~58.94天,滞育雌成虫的平均寿命可达316.24天。雌成虫将大部分卵分散产在寄主附近较高位置的其他物体上,幼虫孵化后吐丝下坠到地面寄主上。蛛网黏结和气流带走导致实验种群中大量的初孵化幼虫死亡。低龄幼虫对寄主的搜索能力不强,野外寄主植物的集中分布对种群生存至关重要。在正常食料条件下,幼虫的龄数是五龄。在食物失水情况下,部分个体增加1次脱皮。幼虫分散栖息,有假死习性,1~3龄期是最容易受到天敌攻击的阶段。越冬雌成虫在3月上、中旬开始产卵后,种群的平均年龄开始下降。从5月下旬至9月上旬前,雌成虫群体中繁殖个体占据大部分,其数量在8月中下旬达到高峰。此后,滞育雌成虫比例逐渐上升,在9月中旬后占据主导地位。2006~2007年间,第1代雌成虫滞育率为8.43~16.11%,第2代的雌成虫滞育率为56.79~78.79%;第3代的雌成虫几乎全部进入滞育。从季节变化来分析,春季滞育率较低,夏季、秋季和冬节滞育率逐渐增高。
在室内采叶饲养条件下,阶段死亡率主要发生在幼虫1~2龄期,其次是3~4~﹡龄和5~6龄期,4~5~﹡龄阶段幼虫死亡率极低。在田间放养条件下,蚂蚁捕食是卵死亡的主要原因。蜘蛛捕食是幼虫死亡的主要原因,其次是蝽象捕食,幼虫疾病很少。幼虫期死亡主要发生在1~2龄阶段,其次是在3~4~﹡龄和4~5~﹡龄阶段。蜘蛛对幼虫的捕食率在年际间较为稳定,而蝽象对幼虫的捕食则年际变化大。各代的存活率曲线均属于典型的Ⅲ型,雨水能减轻捕食性天敌的危害。对于当年繁殖的雌成虫而言,多种大型蜘蛛是主要的捕食性天敌,滞育雌成虫则遭到鼠类的捕食。实验种群各代的性比均接近1:1,各代雌成虫的产卵量受到天气和天敌捕食的影响,存在较大差异。单雌产卵量约350~480粒/雌,卵的孵化率约90%。枯叶蛱蝶具有高繁殖力、高死亡率的r对策类生物的特点。而早期成虫的滞育是枯叶蛱蝶的一种两头下注的重要生活史对策。
不同地理种群成虫在前翅顶角向前外方的突出长度、翅膀宽度和外缘互补角的大小等方面存在差异,可作为鉴别亚种的依据之一。综合形态观测、AFLP分子标记、COⅡ和Cyt b基因片段序列分析的结果,基本支持目前对于枯叶蛱蝶各亚种的划分:①中华亚种Kallima inachus chinensis Swinhoe,包括了长江流域的四川峨眉、重庆江津、湖南东安和江西宜丰,以及福建永泰等地种群;②海南亚种K. i. alicia Joicey & Talbot,分布于海南岛;③西藏墨脱种群可能属于指名亚种Kallima inachus inachus (Doyére);④清迈种群属于暹罗亚种K. i. siamensis Fruhstorfer;⑤日本冲绳种群属于日本亚种K. i. eucerca Fruhstorfer, 1898;⑥基本支持对台湾亚种K. i. formosana Fruhstorfer, 1912的划分。同时,研究结果支持将云南南部的景洪和元江种群划为一个单独的亚种——滇南亚种。在分布于南方热带地区的各亚种之间,仅从翅膀形态上很难进行区分。
枯叶蛱蝶地理种群间的遗传分化程度是很高的,部分种群之间已经达到或超过许多近缘种之间的分化水平,有的可能已处于新种形成的边缘。根据COⅡ和Cyt b基因片段序列分析,推测枯叶蛱蝶可能起源于中南半岛一带,首先向西传播到印度,向北传播到云南和广西南部,向东传播到海南岛。在南方热带地区内各个方向的传播可能在第四纪初或更早之前就已经开始,而进入广西的种群逐渐向北和东北方向传播,到达长江流域各地、福建、台湾和日本冲绳建立现今种群却是较晚的事件。
基于COⅡ和Cyt b基因片段序列差异,各地理种群可以归入两个大组:西藏、泰国、云南和海南等种群可归入“南方种群组”,长江流域、福建、台湾和日本种群可归入“北方种群组”。“南方种群组”内部相互之间以及它们与北方各种群间的序列差异均很大,而北方种群组内部种群间差异较小或很小。
同时,从两个基因序列变异情况看,它们的进化速度适中,适用于枯叶蛱蝶乃至其他蝴蝶的种群分化和亚种界定分析。但对于分歧时间较短的种群分化研究,则Cyt b略强于COⅡ。研究结果有力地证明了分子标记方法,尤其是线粒体基因序列测定在蝴蝶种下分类中的作用。
第四纪冰期和间冰期的反复交替、冷凉暖湿的多重气候旋回与新构造运动的综合作用,对现今枯叶蛱蝶分布区的形成产生了巨大影响。从四川峨眉到日本冲绳的整个北方种群组内的遗传分化程度很低,其原因可能主要有3点:①建立者效应;②定居时间较晚;③相对顺畅的基因交流。
Kallima inachus (Doyére, 1840) (Lepidoptera: Nymphalidae), famous for its mimicry and camouflaging coloration, is of high value in economy, culture and scientific research. Even though it has been divided into 6 subspecies according to the geographic areas of different populations, it’s hard to distinguish them from the external morphology. In addition, the knowledge on its population biology is also lack. The population sizes in many places have decreased, because of habitat loss or quality decline in recent years.
In our study at Emeishan City, Sichuan Province, P. R. China, the experimental population has 3 generations in a year, overwintering by diapause adults. While most females of 1st generation and 2nd generation emerging before mid August go on with their propagation in the year, a few of the females emerging in this period and those emerging after mid August enters reproduction diapause. In fact, the adult overwintering population consists of individuals of 3 generations.
All the activities of adults, such as emerging, feeding, copulating and laying eggs, happen in daytime, closely correlated with sunlight and temperature. In natural habitats, adults take in mainly the sap flowing out of the wounds in trunks or stems of broadleaf trees and rotted fruits, as well as fecaluria of animals sometimes. In the experimental garden, they also take in fresh fruit juice and honey solution. The males show strong territoriality while they are waiting for a female for copulating. If not be preyed by predators, the female adults in diapause could live more than 316 days, while non-diapause females could only live about 36-59 days. Most oftenly, females would rather like to lay most of their eggs dispersedly on the objects around the host plants, such as tree trunks, leaves of shrubs and weeds, only about one third of ova were layed on the upper surface of host leaves. Larva, hatching from the ovum on a higher position, secret a silk drop down onto the ground or right on the leaves of host plants. In that case, a very weak airflow would make the lava deviate from the host plant and some lavae were sticked by spider nets. If host plants are not aboundant in wild, it will be very difficult for 1st to 2nd instar larvae search for host plants.
In condition of excellent foliages of food, the larvae have 5 instars. If the food leaves lost water in high temperature, some of the larvae would experience 6 instars. The larvae would like to live singly on the undersides of host plant leaves throuh 1st to 3rd instars, or on the downward stems and ground near the host through 4th to 5th instar. Encountering a predator, the larvae usually come to mimic death. Anyway, larvae of 1st to 3rd instar are much likely attacked by predators.
In early or mid March, the females after winter begin to lay their eggs, and the average age of experimental population decrease guadually. From late May to early September, most of the female adults in the population go on with their reproduction. After that, the proportion of diapause female rise rapidly. In 2006-2007, while about 8.43~16.11% of female adults in the 1st generations enter diapause, the ratios of female adults in the 2nd and 3rd generations entering diapause are 56.79~78.79% and almost 100% respectively.
Raised indoors with foliages cutted down from the plants, the majority of mortality is that of the 1st to 3rd instar larvae, with far fewer 4th instar larvae getting to death. The last instar larvae seem to be more susceptible to deseases, which are not important to the mortality of the whole generations. When raised dispersally in the field, the main mortality of larvae occurred in the period from 1st to 2nd also, but with many 3rd to 4th instar larvae lost, caused mainly by predators, such as spiders and pentatomid bugs. A typeⅢsurvivorship curve was available in any generation of the experimental population. Most of the adult loss was caused by big spiders, and mice preyed adults overwintering severely.
The sex ratio in each generation of experimental population was approximate to 1:1. About 350 to 480 ova were layed by each female adult, with a hatching rate about 90%. As a r-strategist, the high productive capability compensates its high death, therefore, population can be existed and multiplied.
The length of protrude at the apex and the width of the forewing, in addition with the outer range corner of forewing vary significantly among geographical populations, and these can be used to identify subspecies of Kallima inachus. But it’s not enough. After combining the data taken from the morphology, AFLP, and the sequences of two gene segment, COⅡand Cyt b, we found it’s acceptable to divide the species into 7 subspecies. Firstly, the 6 subspeies identified by previous researchers were proved to be correct. These subspecies are:
1. Kallima inachus chinensis Swinhoe, including populations in Sichuan, Chongqing, Hunan, Jiangxi and Fujian provinces.
2. K. i. alicia Joicey & Talbot, including the population in Hainan Island.
3. K. i. eucerca Fruhstorfer, including the population in Ryukyu Islands.
4. K. i. inachus (Doyére), maybe, including the population at Motuo County in Tibet.
5. K. i. siamensis Fruhstorfer, including the population at Qiangmai, Thailand
6. K. i. formosana Fruhstorfer, including the population in Taiwan Province.
Further more, the study suggest strongly that the population at Jinghong in Yunnan Province should be a subspecies different from any of the frontal ones and this new subspecies should include Yuanjiang population nearby.
Generally, the genetic differentiations among some geographical populations of Kallima inachus are so severe that the levels of variation exceed those among species in other insect taxa. We guess some populations seem to be at the edge of forming new species of the genera. We also guess that Kallima inachus might have originated in Indo-China peninsula millions of years ago, and dispersed north to Yangtze River basin, Taiwan Island and Ryukyu Islands afterwards. Some of the individuals might have gone northwest to India, and some dispersed to Hainan Island during Pleistocene glacial eppoches.
Based on the sequence differentiation of COⅡand Cyt b, the geographical populations studied in this research could be devided into two groups. Populations in Thibet, Thailand, Yunnan and Hainan belong to the southern group, while populations in Yangtze River Basin, Fujian, Taiwan and Ryukyu Islands should belong to the northern group.
研究表明,在四川峨眉,枯叶蛱蝶实验种群一年发生3代,以第1和第2代为主,以滞育成虫越冬。第1代雌成虫和8月中旬前羽化的第2代雌成虫的大部分个体参与当年繁殖,少部分进入生殖滞育。第3代雌成虫和8月中旬后羽化的第2代雌成虫的绝大多数进入生殖滞育。最后,三个世代中的滞育个体汇聚成越冬成虫群体。成虫的羽化、取食、求偶、交配和产卵等活动都在白天进行,且与阳光和气温有密切关系。在野外,成虫的主要补充营养为自阔叶树树干虫蛀伤口中流出的树液和半腐烂的水果,有时也汲食动物粪尿。实验条件下,成虫汲食新鲜果汁、发酵水果、蜂糖水溶液、动物粪便和尿液等。雄成虫的求偶行为属于典型的“等候型”,在求偶时段有强烈的领域性。在不遭受天敌捕食的条件下,繁殖雌成虫的平均寿命为36.67~58.94天,滞育雌成虫的平均寿命可达316.24天。雌成虫将大部分卵分散产在寄主附近较高位置的其他物体上,幼虫孵化后吐丝下坠到地面寄主上。蛛网黏结和气流带走导致实验种群中大量的初孵化幼虫死亡。低龄幼虫对寄主的搜索能力不强,野外寄主植物的集中分布对种群生存至关重要。在正常食料条件下,幼虫的龄数是五龄。在食物失水情况下,部分个体增加1次脱皮。幼虫分散栖息,有假死习性,1~3龄期是最容易受到天敌攻击的阶段。越冬雌成虫在3月上、中旬开始产卵后,种群的平均年龄开始下降。从5月下旬至9月上旬前,雌成虫群体中繁殖个体占据大部分,其数量在8月中下旬达到高峰。此后,滞育雌成虫比例逐渐上升,在9月中旬后占据主导地位。2006~2007年间,第1代雌成虫滞育率为8.43~16.11%,第2代的雌成虫滞育率为56.79~78.79%;第3代的雌成虫几乎全部进入滞育。从季节变化来分析,春季滞育率较低,夏季、秋季和冬节滞育率逐渐增高。
在室内采叶饲养条件下,阶段死亡率主要发生在幼虫1~2龄期,其次是3~4~﹡龄和5~6龄期,4~5~﹡龄阶段幼虫死亡率极低。在田间放养条件下,蚂蚁捕食是卵死亡的主要原因。蜘蛛捕食是幼虫死亡的主要原因,其次是蝽象捕食,幼虫疾病很少。幼虫期死亡主要发生在1~2龄阶段,其次是在3~4~﹡龄和4~5~﹡龄阶段。蜘蛛对幼虫的捕食率在年际间较为稳定,而蝽象对幼虫的捕食则年际变化大。各代的存活率曲线均属于典型的Ⅲ型,雨水能减轻捕食性天敌的危害。对于当年繁殖的雌成虫而言,多种大型蜘蛛是主要的捕食性天敌,滞育雌成虫则遭到鼠类的捕食。实验种群各代的性比均接近1:1,各代雌成虫的产卵量受到天气和天敌捕食的影响,存在较大差异。单雌产卵量约350~480粒/雌,卵的孵化率约90%。枯叶蛱蝶具有高繁殖力、高死亡率的r对策类生物的特点。而早期成虫的滞育是枯叶蛱蝶的一种两头下注的重要生活史对策。
不同地理种群成虫在前翅顶角向前外方的突出长度、翅膀宽度和外缘互补角的大小等方面存在差异,可作为鉴别亚种的依据之一。综合形态观测、AFLP分子标记、COⅡ和Cyt b基因片段序列分析的结果,基本支持目前对于枯叶蛱蝶各亚种的划分:①中华亚种Kallima inachus chinensis Swinhoe,包括了长江流域的四川峨眉、重庆江津、湖南东安和江西宜丰,以及福建永泰等地种群;②海南亚种K. i. alicia Joicey & Talbot,分布于海南岛;③西藏墨脱种群可能属于指名亚种Kallima inachus inachus (Doyére);④清迈种群属于暹罗亚种K. i. siamensis Fruhstorfer;⑤日本冲绳种群属于日本亚种K. i. eucerca Fruhstorfer, 1898;⑥基本支持对台湾亚种K. i. formosana Fruhstorfer, 1912的划分。同时,研究结果支持将云南南部的景洪和元江种群划为一个单独的亚种——滇南亚种。在分布于南方热带地区的各亚种之间,仅从翅膀形态上很难进行区分。
枯叶蛱蝶地理种群间的遗传分化程度是很高的,部分种群之间已经达到或超过许多近缘种之间的分化水平,有的可能已处于新种形成的边缘。根据COⅡ和Cyt b基因片段序列分析,推测枯叶蛱蝶可能起源于中南半岛一带,首先向西传播到印度,向北传播到云南和广西南部,向东传播到海南岛。在南方热带地区内各个方向的传播可能在第四纪初或更早之前就已经开始,而进入广西的种群逐渐向北和东北方向传播,到达长江流域各地、福建、台湾和日本冲绳建立现今种群却是较晚的事件。
基于COⅡ和Cyt b基因片段序列差异,各地理种群可以归入两个大组:西藏、泰国、云南和海南等种群可归入“南方种群组”,长江流域、福建、台湾和日本种群可归入“北方种群组”。“南方种群组”内部相互之间以及它们与北方各种群间的序列差异均很大,而北方种群组内部种群间差异较小或很小。
同时,从两个基因序列变异情况看,它们的进化速度适中,适用于枯叶蛱蝶乃至其他蝴蝶的种群分化和亚种界定分析。但对于分歧时间较短的种群分化研究,则Cyt b略强于COⅡ。研究结果有力地证明了分子标记方法,尤其是线粒体基因序列测定在蝴蝶种下分类中的作用。
第四纪冰期和间冰期的反复交替、冷凉暖湿的多重气候旋回与新构造运动的综合作用,对现今枯叶蛱蝶分布区的形成产生了巨大影响。从四川峨眉到日本冲绳的整个北方种群组内的遗传分化程度很低,其原因可能主要有3点:①建立者效应;②定居时间较晚;③相对顺畅的基因交流。
Kallima inachus (Doyére, 1840) (Lepidoptera: Nymphalidae), famous for its mimicry and camouflaging coloration, is of high value in economy, culture and scientific research. Even though it has been divided into 6 subspecies according to the geographic areas of different populations, it’s hard to distinguish them from the external morphology. In addition, the knowledge on its population biology is also lack. The population sizes in many places have decreased, because of habitat loss or quality decline in recent years.
In our study at Emeishan City, Sichuan Province, P. R. China, the experimental population has 3 generations in a year, overwintering by diapause adults. While most females of 1st generation and 2nd generation emerging before mid August go on with their propagation in the year, a few of the females emerging in this period and those emerging after mid August enters reproduction diapause. In fact, the adult overwintering population consists of individuals of 3 generations.
All the activities of adults, such as emerging, feeding, copulating and laying eggs, happen in daytime, closely correlated with sunlight and temperature. In natural habitats, adults take in mainly the sap flowing out of the wounds in trunks or stems of broadleaf trees and rotted fruits, as well as fecaluria of animals sometimes. In the experimental garden, they also take in fresh fruit juice and honey solution. The males show strong territoriality while they are waiting for a female for copulating. If not be preyed by predators, the female adults in diapause could live more than 316 days, while non-diapause females could only live about 36-59 days. Most oftenly, females would rather like to lay most of their eggs dispersedly on the objects around the host plants, such as tree trunks, leaves of shrubs and weeds, only about one third of ova were layed on the upper surface of host leaves. Larva, hatching from the ovum on a higher position, secret a silk drop down onto the ground or right on the leaves of host plants. In that case, a very weak airflow would make the lava deviate from the host plant and some lavae were sticked by spider nets. If host plants are not aboundant in wild, it will be very difficult for 1st to 2nd instar larvae search for host plants.
In condition of excellent foliages of food, the larvae have 5 instars. If the food leaves lost water in high temperature, some of the larvae would experience 6 instars. The larvae would like to live singly on the undersides of host plant leaves throuh 1st to 3rd instars, or on the downward stems and ground near the host through 4th to 5th instar. Encountering a predator, the larvae usually come to mimic death. Anyway, larvae of 1st to 3rd instar are much likely attacked by predators.
In early or mid March, the females after winter begin to lay their eggs, and the average age of experimental population decrease guadually. From late May to early September, most of the female adults in the population go on with their reproduction. After that, the proportion of diapause female rise rapidly. In 2006-2007, while about 8.43~16.11% of female adults in the 1st generations enter diapause, the ratios of female adults in the 2nd and 3rd generations entering diapause are 56.79~78.79% and almost 100% respectively.
Raised indoors with foliages cutted down from the plants, the majority of mortality is that of the 1st to 3rd instar larvae, with far fewer 4th instar larvae getting to death. The last instar larvae seem to be more susceptible to deseases, which are not important to the mortality of the whole generations. When raised dispersally in the field, the main mortality of larvae occurred in the period from 1st to 2nd also, but with many 3rd to 4th instar larvae lost, caused mainly by predators, such as spiders and pentatomid bugs. A typeⅢsurvivorship curve was available in any generation of the experimental population. Most of the adult loss was caused by big spiders, and mice preyed adults overwintering severely.
The sex ratio in each generation of experimental population was approximate to 1:1. About 350 to 480 ova were layed by each female adult, with a hatching rate about 90%. As a r-strategist, the high productive capability compensates its high death, therefore, population can be existed and multiplied.
The length of protrude at the apex and the width of the forewing, in addition with the outer range corner of forewing vary significantly among geographical populations, and these can be used to identify subspecies of Kallima inachus. But it’s not enough. After combining the data taken from the morphology, AFLP, and the sequences of two gene segment, COⅡand Cyt b, we found it’s acceptable to divide the species into 7 subspecies. Firstly, the 6 subspeies identified by previous researchers were proved to be correct. These subspecies are:
1. Kallima inachus chinensis Swinhoe, including populations in Sichuan, Chongqing, Hunan, Jiangxi and Fujian provinces.
2. K. i. alicia Joicey & Talbot, including the population in Hainan Island.
3. K. i. eucerca Fruhstorfer, including the population in Ryukyu Islands.
4. K. i. inachus (Doyére), maybe, including the population at Motuo County in Tibet.
5. K. i. siamensis Fruhstorfer, including the population at Qiangmai, Thailand
6. K. i. formosana Fruhstorfer, including the population in Taiwan Province.
Further more, the study suggest strongly that the population at Jinghong in Yunnan Province should be a subspecies different from any of the frontal ones and this new subspecies should include Yuanjiang population nearby.
Generally, the genetic differentiations among some geographical populations of Kallima inachus are so severe that the levels of variation exceed those among species in other insect taxa. We guess some populations seem to be at the edge of forming new species of the genera. We also guess that Kallima inachus might have originated in Indo-China peninsula millions of years ago, and dispersed north to Yangtze River basin, Taiwan Island and Ryukyu Islands afterwards. Some of the individuals might have gone northwest to India, and some dispersed to Hainan Island during Pleistocene glacial eppoches.
Based on the sequence differentiation of COⅡand Cyt b, the geographical populations studied in this research could be devided into two groups. Populations in Thibet, Thailand, Yunnan and Hainan belong to the southern group, while populations in Yangtze River Basin, Fujian, Taiwan and Ryukyu Islands should belong to the northern group.
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