同域分布共享传粉者的鼠尾草属植物的生殖隔离
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摘要
生殖隔离是生物多样性产生的重要原因之一,不同物种间的生殖隔离形成阶段、方式和强度不完全相同。为了揭示生殖隔离在鼠尾草属(Salvia)物种多样性产生和维持过程中的作用和特点,本文研究了浙江天目山同域分布的舌瓣鼠尾草(S.liguliloba)和南丹参(S.bowleyana)的开花、传粉和生殖隔离,利用人工授粉和杂交实验检测它们的种间遗传相容程度。结果表明,在花的形态结构、花及花序的生长、着生方式与数量特征上,2种鼠尾草属植物均差异显著(P<0.05)。2种鼠尾草属植物共享同一种有效传粉昆虫——三条熊蜂(Bombus trifasciatus),但通过访花行为的显著差异和明显不同的花粉落置部位,有效避免了异源花粉干扰。人工杂交授粉的结果表明2个物种间遗传相容性较高,互为亲本的杂交结实率分别达到77.8±10.7%和78.7±11.2%。我们的研究表明,同域分布、花期重叠且共享唯一传粉者的2种鼠尾草属植物,以花部的传粉结构和传粉部位的差异,产生了较高程度的传粉前生殖隔离,避免了物种间的异源花粉干扰和自然杂交,保障各自较高的繁殖成效,以维持自然种群的多样性和遗传结构的稳定。
Reproductive isolation(RI) is one of the key factors for speciation and diversity maintenance, however, there are differences in formation stage, means, and strength of RI for different species. To assess the effects and the significance of reproductive isolation in Salvia species, we compared flowering, pollination, and reproduction characteristics of Salvia liguliloba and S. bowleyana, which grow sympatrically and have overlapping flowering periods in the Tianmu Mountain, Zhejiang. Furthermore, artificial hybridization between the two species were conducted to estimate and understand their genetic compatibility and reproductive isolation. Results indicated that the two Salvia species considerably differed in their flower morphological structures, inflorescence organization, and the number of flowers produced per inflorescence. Bombus trifasciatus is the sole pollinator for these two species during the overlapping flowering period. However, different visitation behavior and floral structure(P < 0.05) leads to obviously different pollination patterns between the two species. Pollen is deposited on distinctly separate areas of the pollinator's body in a manner precluding contact with any heterospecific Salvia stigmata. Under natural condition, the two species are equally successful in reproduction(natural seed set > 87%). Artificial pollination and hybridization experiments between these two species showed that they have a higher genetic compatibility. The cross seed sets are 77.8 ± 10.7% and 78.7 ± 11.2% when the two species are reciprocally cross parents. Our research suggests that for the two Salvia species lacking genetic incompatibility systems and relying on pollinators for outcrossing, there are differences in floral structures and pollen placement sites. The mechanical isolation(a form of pre-pollination RI) prevents heterospecific pollen interference and natural hybridization of the two different species that grow sympatrically and have overlapping flowering periods, and also maintains species diversity and the constancy of species heredity.
Reproductive isolation(RI) is one of the key factors for speciation and diversity maintenance, however, there are differences in formation stage, means, and strength of RI for different species. To assess the effects and the significance of reproductive isolation in Salvia species, we compared flowering, pollination, and reproduction characteristics of Salvia liguliloba and S. bowleyana, which grow sympatrically and have overlapping flowering periods in the Tianmu Mountain, Zhejiang. Furthermore, artificial hybridization between the two species were conducted to estimate and understand their genetic compatibility and reproductive isolation. Results indicated that the two Salvia species considerably differed in their flower morphological structures, inflorescence organization, and the number of flowers produced per inflorescence. Bombus trifasciatus is the sole pollinator for these two species during the overlapping flowering period. However, different visitation behavior and floral structure(P < 0.05) leads to obviously different pollination patterns between the two species. Pollen is deposited on distinctly separate areas of the pollinator's body in a manner precluding contact with any heterospecific Salvia stigmata. Under natural condition, the two species are equally successful in reproduction(natural seed set > 87%). Artificial pollination and hybridization experiments between these two species showed that they have a higher genetic compatibility. The cross seed sets are 77.8 ± 10.7% and 78.7 ± 11.2% when the two species are reciprocally cross parents. Our research suggests that for the two Salvia species lacking genetic incompatibility systems and relying on pollinators for outcrossing, there are differences in floral structures and pollen placement sites. The mechanical isolation(a form of pre-pollination RI) prevents heterospecific pollen interference and natural hybridization of the two different species that grow sympatrically and have overlapping flowering periods, and also maintains species diversity and the constancy of species heredity.
引文
Baack E,Melo MC,Rieseberg LH,Ortiz-Barrientos D(2015)The origins of reproductive isolation in plants.New Phytologist,207,968-984.
Cla?en-Bockhoff R,Speck T,Tweraser E,Wester P,Thimm S,Reith M(2004)The staminal lever mechanism in Salvia L.(Lamiaceae):a key innovation for adaptive radiation?Organisms Diversity&Evolution,4,189-205.
Cla?en-Bockhoff R,Wester P,Tweraser E(2003)The staminal lever mechanism in Salvia L.(Lamiaceae):a review.Plant Biology,5,33-41.
Epling C(1947)Natural hybridization of Salvia apiana and S.mellifera.Evolution,1,69-78.
Hopkins R(2013)Reinforcement in plants.New Phytologist,197,1095-1103.
Huang S,Shi X(2013)Floral isolation in Pedicularis:how do congeners with shared pollinators minimize reproductive interference?New Phytologist,199,858-865.
Huang YB,Wei YK,Ge BJ,Wang Q(2014)Research progress in pollination biology of genus Salvia(Lamiaceae)and their pollination mechanisms in East Asia(China).Acta Ecologica Sinica,34,2282-2289.(in Chinese with English abstract)[黄艳波,魏宇昆,葛斌杰,王琦(2014)鼠尾草属东亚分支的传粉模式.生态学报,34,2282-2289.]
Huang YB,Wei YK,Wang Q,Xiao YE,Ye XY(2015)Floral morphology and pollination mechanism of Salvia liguliloba,a narrow endemic species with degraded lever-like stamens.Chinese Journal of Plant Ecology,39,753-761.(in Chinese with English abstract)[黄艳波,魏宇昆,王琦,肖月娥,叶喜阳(2015)舌瓣鼠尾草退化杠杆雄蕊的相关花部特征及传粉机制.植物生态学报,39,753-761.]
Huang Z,Liu H,Huang S(2015)Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body.Journal of Plant Ecology,8,109-115.
Kipling R,Warren J(2013)How generalists coexist:the role of floral phenotype and spatial factors in the pollination systems of two Ranunculus species.Journal of Plant Ecology,7,480-489.
Ma YP,Xie WJ,Sun WB,Marczewski T(2016a)Strong reproductive isolation despite occasional hybridization between a widely distributed and a narrow endemic Rhododendron species.Scientific Reports,6,19146.
Ma YP,Zhou RC,Milne R(2016b)Pollinator-mediated isolation may be an underestimated factor in promoting homoploid hybrid speciation.Frontiers in Plant Science,7,1183.
Melo MC,Grealy A,Brittain B,Walter GM,Ortiz-Barrientos D(2014)Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel.New Phytologist,203,323-334.
Meyn O,Emboden WA(1987)Parameters and consequences of introgression in Salvia apiana×S.mellifera(Lamiaceae).Systematic Botany,12,390-399.
Pauw A(2013)Can pollination niches facilitate plant coexistence?Trends in Ecology&Evolution,28,30-37.
Pedron M,Buzatto CR,Singer RB,Batista JAN,Moser A(2012)Pollination biology of four sympatric species of Habenaria(Orchidaceae:Orchidinae)from southern Brazil.Botanical Journal of the Linnean Society,170,141-156.
Ruchisansakun S,Tangtorwongsakul P,Cozien RJ,Smets EF,Niet TVD(2016)Floral specialization for different pollinators and divergent use of the same pollinator among co-occuring Impatiens species(Balsaminaceae)from Southeast Asia.Botanical Journal of the Linnean Society,181,651-666.
Wei YK,Wang Q,Huang YB(2015)Species diversity and distribution of Salvia(Lamiaceae).Biodiversity Science,23,3-10.(in Chinese with English abstract)[魏宇昆,王琦,黄艳波(2015)唇形科鼠尾草属的物种多样性与分布.生物多样性,23,3-10.]
Wester P,Cla?en-Bockhoff R(2007)Floral diversity and pollen transfer mechanisms in bird-pollinated Salvia species.Annals of Botany,100,401-421.
Widmer A,Lexer C,Cozzolino S(2009)Evolution of reproductive isolation in plants.Heredity,102,31-38.
Yang FC(1992)Comprehensive Investigation Report on Natural Resource of Tianmu Mountain Nature Reserve.Zhejiang Science and Technology Press,Hangzhou.(in Chinese)[杨逢春(1992)天目山自然保护区自然资源综合考察报告.浙江科学技术出版社,杭州.]
Cla?en-Bockhoff R,Speck T,Tweraser E,Wester P,Thimm S,Reith M(2004)The staminal lever mechanism in Salvia L.(Lamiaceae):a key innovation for adaptive radiation?Organisms Diversity&Evolution,4,189-205.
Cla?en-Bockhoff R,Wester P,Tweraser E(2003)The staminal lever mechanism in Salvia L.(Lamiaceae):a review.Plant Biology,5,33-41.
Epling C(1947)Natural hybridization of Salvia apiana and S.mellifera.Evolution,1,69-78.
Hopkins R(2013)Reinforcement in plants.New Phytologist,197,1095-1103.
Huang S,Shi X(2013)Floral isolation in Pedicularis:how do congeners with shared pollinators minimize reproductive interference?New Phytologist,199,858-865.
Huang YB,Wei YK,Ge BJ,Wang Q(2014)Research progress in pollination biology of genus Salvia(Lamiaceae)and their pollination mechanisms in East Asia(China).Acta Ecologica Sinica,34,2282-2289.(in Chinese with English abstract)[黄艳波,魏宇昆,葛斌杰,王琦(2014)鼠尾草属东亚分支的传粉模式.生态学报,34,2282-2289.]
Huang YB,Wei YK,Wang Q,Xiao YE,Ye XY(2015)Floral morphology and pollination mechanism of Salvia liguliloba,a narrow endemic species with degraded lever-like stamens.Chinese Journal of Plant Ecology,39,753-761.(in Chinese with English abstract)[黄艳波,魏宇昆,王琦,肖月娥,叶喜阳(2015)舌瓣鼠尾草退化杠杆雄蕊的相关花部特征及传粉机制.植物生态学报,39,753-761.]
Huang Z,Liu H,Huang S(2015)Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body.Journal of Plant Ecology,8,109-115.
Kipling R,Warren J(2013)How generalists coexist:the role of floral phenotype and spatial factors in the pollination systems of two Ranunculus species.Journal of Plant Ecology,7,480-489.
Ma YP,Xie WJ,Sun WB,Marczewski T(2016a)Strong reproductive isolation despite occasional hybridization between a widely distributed and a narrow endemic Rhododendron species.Scientific Reports,6,19146.
Ma YP,Zhou RC,Milne R(2016b)Pollinator-mediated isolation may be an underestimated factor in promoting homoploid hybrid speciation.Frontiers in Plant Science,7,1183.
Melo MC,Grealy A,Brittain B,Walter GM,Ortiz-Barrientos D(2014)Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel.New Phytologist,203,323-334.
Meyn O,Emboden WA(1987)Parameters and consequences of introgression in Salvia apiana×S.mellifera(Lamiaceae).Systematic Botany,12,390-399.
Pauw A(2013)Can pollination niches facilitate plant coexistence?Trends in Ecology&Evolution,28,30-37.
Pedron M,Buzatto CR,Singer RB,Batista JAN,Moser A(2012)Pollination biology of four sympatric species of Habenaria(Orchidaceae:Orchidinae)from southern Brazil.Botanical Journal of the Linnean Society,170,141-156.
Ruchisansakun S,Tangtorwongsakul P,Cozien RJ,Smets EF,Niet TVD(2016)Floral specialization for different pollinators and divergent use of the same pollinator among co-occuring Impatiens species(Balsaminaceae)from Southeast Asia.Botanical Journal of the Linnean Society,181,651-666.
Wei YK,Wang Q,Huang YB(2015)Species diversity and distribution of Salvia(Lamiaceae).Biodiversity Science,23,3-10.(in Chinese with English abstract)[魏宇昆,王琦,黄艳波(2015)唇形科鼠尾草属的物种多样性与分布.生物多样性,23,3-10.]
Wester P,Cla?en-Bockhoff R(2007)Floral diversity and pollen transfer mechanisms in bird-pollinated Salvia species.Annals of Botany,100,401-421.
Widmer A,Lexer C,Cozzolino S(2009)Evolution of reproductive isolation in plants.Heredity,102,31-38.
Yang FC(1992)Comprehensive Investigation Report on Natural Resource of Tianmu Mountain Nature Reserve.Zhejiang Science and Technology Press,Hangzhou.(in Chinese)[杨逢春(1992)天目山自然保护区自然资源综合考察报告.浙江科学技术出版社,杭州.]