贡嘎山高低海拔上优势杨柳科植物性别比例与繁殖特性
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摘要
雌雄异株植物的性比问题一直是进化生物学的研究热点之一.为揭示杨柳科植物不同性比格局的内在机理,从繁殖投入、种群密度和传粉效率等方面对贡嘎山两个海拔高度(2 000和2 600 m)上冬瓜杨和川滇柳的性别比例与繁殖投入进行对比研究.结果显示:(1)低海拔下冬瓜杨和川滇柳雄雌性比(M/F)接近1:1平衡;而在高海拔区域出现性比失衡,即杨树偏雄(M/F=2.36,P=0.008),而柳树偏雌(M/F=0.62,P=0.033).(2)冬瓜杨和川滇柳种群密度随海拔升高均明显下降,但川滇柳密度显著高于冬瓜杨,柱头接收花粉数量亦显著高于冬瓜杨.(3)枝条水平上,杨柳的总繁殖结构生物量(花序干重+种子干重)在两个海拔上都为雌株高于雄株;相对繁殖投入在低海拔时雌株高于雄株,高海拔上冬瓜杨雌株高于雄株,而川滇柳由于叶片的补偿生长,包括更高的叶片生物量投入和光合能力,导致相对繁殖投入雌雄间无显著差异.冬瓜杨雌株繁殖投入显著高于雄株,雌株对高海拔更敏感,因而高海拔时偏雄性.川滇柳的繁殖投入在海拔间无差异,加之传粉效率较高,可能容易产生花粉管竞争,从而偏雌性.本研究发现较之低海拔,贡嘎山上杨柳科植物在高海拔上叶与繁殖结构生物量权衡关系改变容易导致性比失衡,未来需在分子水平上,结合性别决定基因、性染色体和表观遗传学等进一步深入研究.
The causes and consequences of variation in the sex ratios of organisms with separate sexes remain a central theme in evolutionary biology. The sex ratios of sympatric Populus sp. and Salix sp. vary according to the altitude and species; 1:1 equilibrium sex ratios are observed at mid-altitudes while the ratios are skewed at high altitudes, with Populus sp. having male-biased and Salix sp. having female-biased sex ratios. In this study, the reproductive investments, population density, and pollination efficiency of P. purdomii and S. magnifica were assessed at two different altitudes of 2 000 and 2 600 m on the Gongga Mountain, with the aim to provide new clues on the ecological and evolutionary aspects of the two species. Our results showed that the population densities significantly decreased from 2 000 to 2 600 m, being higher for S. magnificathan for P. purdomii at both the altitudes. The pollen received by the stigma was also significantly higher in Salix sp., due to its high population density, as well as due to the simultaneous pollination by the wind and insects, which may intensify the gametophytic competition to favor selective fertilization by the female-determining pollen tubes. Reproductive investments, including the biomass of the inflorescence and the seeds was higher in the females of Populus sp. at both the altitudes, whereas for Salix sp., the biomass was higher in the females at low altitudes, and was comparable to those at high altitudes. Under conditions of optimal temperature and precipitation, vigorous plant growth combined with relatively smaller reproductive investments was observed to contribute to the 1:1 equilibrium sex ratio, at an altitude of 2 000 m. At higher altitudes, the balance between the reproductive and vegetative growth was easily affected by more pronounced gender-related differences for reproduction, resulting in biased sex ratios, e.g.: Populus sp. exhibited male biasness and Salix sp. showed female biasness at high altitudes. Consequently, our results improve our understanding of the causes and consequences of sexual dimorphism in dioecious species. However, more information on the genetic or epigenetic basis of sex determination, including identification of the definite sex chromosomes and sex markers is urgently needed.
The causes and consequences of variation in the sex ratios of organisms with separate sexes remain a central theme in evolutionary biology. The sex ratios of sympatric Populus sp. and Salix sp. vary according to the altitude and species; 1:1 equilibrium sex ratios are observed at mid-altitudes while the ratios are skewed at high altitudes, with Populus sp. having male-biased and Salix sp. having female-biased sex ratios. In this study, the reproductive investments, population density, and pollination efficiency of P. purdomii and S. magnifica were assessed at two different altitudes of 2 000 and 2 600 m on the Gongga Mountain, with the aim to provide new clues on the ecological and evolutionary aspects of the two species. Our results showed that the population densities significantly decreased from 2 000 to 2 600 m, being higher for S. magnificathan for P. purdomii at both the altitudes. The pollen received by the stigma was also significantly higher in Salix sp., due to its high population density, as well as due to the simultaneous pollination by the wind and insects, which may intensify the gametophytic competition to favor selective fertilization by the female-determining pollen tubes. Reproductive investments, including the biomass of the inflorescence and the seeds was higher in the females of Populus sp. at both the altitudes, whereas for Salix sp., the biomass was higher in the females at low altitudes, and was comparable to those at high altitudes. Under conditions of optimal temperature and precipitation, vigorous plant growth combined with relatively smaller reproductive investments was observed to contribute to the 1:1 equilibrium sex ratio, at an altitude of 2 000 m. At higher altitudes, the balance between the reproductive and vegetative growth was easily affected by more pronounced gender-related differences for reproduction, resulting in biased sex ratios, e.g.: Populus sp. exhibited male biasness and Salix sp. showed female biasness at high altitudes. Consequently, our results improve our understanding of the causes and consequences of sexual dimorphism in dioecious species. However, more information on the genetic or epigenetic basis of sex determination, including identification of the definite sex chromosomes and sex markers is urgently needed.
引文
1 Renner SS,Ricklefs RE.Dioecy and its correlates in the flowering plants[J].Am J Bot,1995,82(5):596-606.
2 Fisher RA.The Genetical Theory of Natural Selection[M].Oxford:Oxford University Press,1930
3尹春英,李春阳.雌雄异株植物与性别比例有关的性别差异研究现状与展望[J].应用与环境生物学报,2007,13(3):419-425[Yin CY,Li CY.Gender differences of dioecious plants related sex ratio recent advances and future prospects[J].Chin J Appl Environ Biol,2007,13(3):419-425]
4陈娟,李春阳.环境胁迫下雌雄异株植物的性别响应差异及竞争关系[J].应用与环境生物学报,2014,20(4):743-750[Chen J,Li CY.Sexspecific responses to environmental stresses and sexual competition of dioecious plants[J].Chin J Appl Environ Biol,2014,20(4):743-750]
5 Correial O,Barradas MCD.Ecophysiological differences between male and female plants of Pistacia lentiscus L.[J].Plant Ecol,2000,149:131-142
6 Freeman DC,Klikoff LG,Harper KT.Differential resource utilization by the sexes of dioecious plants[J].Science,1976,193:597-599
7 Li C,Xu G,Zang R,Korpelainen H,Berninger F.Sex-related differences i n leaf mor pholog ical a nd physiolog ical responses i n Hippophae rhamnoides along an altitudinal gradient[J].Tree Physiol,2007,27(3):399-406
8 Or tiz PL,A r ista M,Talavera S.Sex ratio and reproductive effor t in the dioecious Juniper us communis subsp.alpina(Suter)?elak.(Cupressaceae)along an altitudinal gradient[J].Ann Bot,2002,89(2):205-211
9王志峰,胥晓,李霄峰,杨鹏,袁新利.青杨雌雄群体沿海拔梯度的分布特征[J].生态学报,2011,31(23):7067-7074[Wang ZF,Xu X,Li XF,Yang P,Yuan XL.The distribution of male and female Populus cathayana populations along an altitudinal gradient[J].Acta Ecol Sin,2011,31(23):7067-7074]
10 Grant MC,Mitton JB.Elevational gradients in adult sex ratios and sexual differentiation in vegetative growth rates of Populus tremuloides Michx[J].Evolution,1979,33:914-918
11 Ueno N,Suyama Y,Seiwa K.What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis?[J].J Ecol,2007,95(5):951-959
12 Myers-smith IH,Hikd S.Uniform female-biased sex ratios in alpine willows[J].Am J Bot,2012,99(7):1243-1248
13 Fabbro T,K?rener C.Altit udinal differences in f lower t raits and reproductive allocation[J].Flora-Morphol Distr Funct Ecol Plants,2004,199(1):70-81
14 Guo H,Weiner J,Mazer SJ,Zhao ZG,Du GZ,Li B.Reproductive allometry in Pedicularis species changes with elevation[J].J Ecol,2012,100(2):452-458
15 Zhang L,Luo TX,Liu XS,Wang Y.Altit udinal var iation in leaf construction cost and energy content of Bergenia purpurascens[J].Acta Oecol,2012,43:72-79
16 Lei YB,Chen K,Jiang H,Yu L,Duan BL.Contrasting responses in the growth and energy utilization properties of sympatric Populus and Salix to different altitudes:implications for sexual dimorphism in Salicaceae[J].Physiol Plant,2017,159(1):30-41
17 Cor rens C.The concur rence of male on female ger m cells and the numerical proportion of both genders[J].Naturwissenschaften,1918,6:277-280
18冯毅,王朱涛,蔡应君,任树平,柴成忠,罗建勋.川西北地区康定柳天然群体表型多样性研究[J].西南林学院学院,2010,30:11-20[Feng Y,Wang ZT,Cai YJ,Ren SP,Chai CZ,Luo JX.Study on phenotypic diversity of Salix paraplesia natural populations in northwest Sichuan[J].J SW For Univ,2010,30:11-20]
19李超男,李家宝,李香真.贡嘎山海拔梯度上不同植被类型土壤甲烷氧化菌群落结构及多样性[J].应用生态学报,2017,28(3):805-814[Li CN,Li JB,Li XZ.Soil methanotrophic community structure and diversity in different vegetation types at elevation gradient of Gongga Mountain,Southwest China[J].Chin J Appl Ecol,2017,28(3):805-814]
20 Bing HJ,Wu YH,Zhou J,Sun HY,Luo J,Wang JP,Yu D.Stoichiometric variation of carbon,nitrogen and phosphorus in soils and its implication for nutrient limitation in alpine ecosystem of eastern Tibetan Plateau[J].J Soils Sed,2016,16:405-416
21 Sun H,Wu Y,Yu D,Zhou J.Altitudinal gradient of microbial biomass phosphor us a nd it s relat ionsh ip w it h m icrobial biomass ca rbon,nitrogen,and rhizosphere soil phosphor us on the easter n slope of Gongga Mountain,SW China[J].PLo S ONE,2013,8(9):e72952
22周俊,邴海健,吴艳宏,孙守琴,罗辑.贡嘎山燕子沟土壤磷海拔梯度特征及影响因素[J].山地学报,2016,34(4):385-392[Zhou J,Bing HJ,Wu YH,Sun SQ,Luo J.Variations in soil P biogeochemistry and its impact factors along an altitudinal gradient in the Yanzigou,eastern slope of the Gongga Mountain[J].Mount Res,2016,34(4):385-392]
23徐庆,姜春前,刘世荣,郭泉水.濒危植物四合木种群传粉生态学研究[J].林业科学院研究,2003,16:391-397[Xu Q,Jiang CQ,Liu SR,Guo QS.Study on pollination ecology of endangered plant Tetraena mongolica population[J].For Res,2003,16:391-397]
24 Petzold A,Pfeiffer T,Jansen F,Eusemann P,Schnittler M.Sex ratios and clonal growth in dioecious Populus euphratica Oliv.,Xinjiang Prov.,western China.Trees-Struct Funct,2013,27(3):729-744
25 Che-Castaldo C,Crisafulli CM,Bishop JG,Fagan WF.What causes female bias in the secondary sex ratios of the dioecious woody shrub Salix sitchensis colonizing a primary successional landscape?[J].Am JBot,2015,102(8),1309-1322
26 Obeso J.The costs of reproduction in plants[J].New Phytol,2002,155:321-348
27 Ishida TA,Hattori K,Shibata S,Suzuki M,Kimura MT.Sex allocation of a cosexual wind-pollinated tree,Quercus dentata,in terms of four currencies[J].J Plant Res,2005,118(3):193-197
28李嘉竹,王国安,刘贤赵,韩家懋,刘敏,柳晓娟.贡嘎山东坡C3植物碳同位素组成及C4植物沿海拔高度的变化[J].中国科学D辑:地球科学,2009,39(10):1387-1396[Li JZ,Wang GA,Liu XZ,Han JM,Liu M,Liu XJ.Variations in carbon isotope ratios of C3 plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga[J].Sci China Ser D Earth Sci,2009,39(10):1387-1396]
29 Field DL,Pickup M,Barrett SCH.The influence of pollination intensity on fer tilization success,progeny sex ratio,and f it ness in a windpollinated,dioecious plant[J].Intern J Plant Sci,2012,173(2):184-191
30 Sinclair JP,Emlen J,Freeman DC.Biased sex ratios in plants:theory and trends[J].Bot Rev,2012,78(1):63-86
31 He JD,Dong TF,Huang KC,Yang YX,Li DD,Xu X,He XH.Sexspecific f loral morphology,biomass,and phytohormones associated with altitude in dioecious Populus cathayana populations[J].Ecol Evol,2017,7(11):3976-3986
32 Geraldes A,Hefer CA,Capron A,Kolosova N,Mar tinez-Nu?ez F,Soolanayakanahally RY,Stanton B,Guy RD,Mansfield SD,Douglas CJ,Cronk QCB.Recent Y chromosome divergence despite ancient origin of dioecy in poplars(Populus)[J].Mol Ecol,2015,24(13):3243-3256
33张林静,石云霞,潘晓玲.草本植物繁殖分配与海拔高度的相关分析[J].西北大学学报:自然科学版,2007,37(1):77-80[Zhang LJ,Shi YX,Pan XL.Analysis of correlativity between reproductive allocation and altitude in plants[J].J NW Univ(Nat Sci Ed),2007,37(1):77-90]
34王一峰,刘启茜,裴泽宇,李海燕.青藏高原3种风毛菊属植物的繁殖分配与海拔高度的相关性[J].植物生态学报,2012,36(1):39-46[Wang YF,Liu QQ,Pei ZY,Li HY.Correlation between altitude and reproductive allocation in three Saussurea species on China’s QinghaiTibetan Plateau[J].Chin J Plant Ecol,2012,36(1):39-46]
35樊宝丽,孟金柳,赵志刚,杜国祯.海拔对青藏高原东部毛茛科植物繁殖特征和资源分配的影响[J].西北植物学报,2008,28(4):805-811[Fan BL,Meng JL,Zhao ZG,Du GZ.Influence of altitude on reproductive traits and resource allocation of species of ranunculaceae at East Qinghai Tibetan Plateu[J].Acta Bot Bor-Occid Sin,2008,28(4):805-811]
36苏梅.青藏高原东部高寒草甸九种常见植物叶特征、繁殖特征研究[D].兰州:兰州大学,2009[Su M.Leaf trait and reproductive traits of nine common species of plants at eastern alpine meadow in QinhaiTibetan Plateu[D].Lanzhou:Lanzhou Universtiy,2009]
2 Fisher RA.The Genetical Theory of Natural Selection[M].Oxford:Oxford University Press,1930
3尹春英,李春阳.雌雄异株植物与性别比例有关的性别差异研究现状与展望[J].应用与环境生物学报,2007,13(3):419-425[Yin CY,Li CY.Gender differences of dioecious plants related sex ratio recent advances and future prospects[J].Chin J Appl Environ Biol,2007,13(3):419-425]
4陈娟,李春阳.环境胁迫下雌雄异株植物的性别响应差异及竞争关系[J].应用与环境生物学报,2014,20(4):743-750[Chen J,Li CY.Sexspecific responses to environmental stresses and sexual competition of dioecious plants[J].Chin J Appl Environ Biol,2014,20(4):743-750]
5 Correial O,Barradas MCD.Ecophysiological differences between male and female plants of Pistacia lentiscus L.[J].Plant Ecol,2000,149:131-142
6 Freeman DC,Klikoff LG,Harper KT.Differential resource utilization by the sexes of dioecious plants[J].Science,1976,193:597-599
7 Li C,Xu G,Zang R,Korpelainen H,Berninger F.Sex-related differences i n leaf mor pholog ical a nd physiolog ical responses i n Hippophae rhamnoides along an altitudinal gradient[J].Tree Physiol,2007,27(3):399-406
8 Or tiz PL,A r ista M,Talavera S.Sex ratio and reproductive effor t in the dioecious Juniper us communis subsp.alpina(Suter)?elak.(Cupressaceae)along an altitudinal gradient[J].Ann Bot,2002,89(2):205-211
9王志峰,胥晓,李霄峰,杨鹏,袁新利.青杨雌雄群体沿海拔梯度的分布特征[J].生态学报,2011,31(23):7067-7074[Wang ZF,Xu X,Li XF,Yang P,Yuan XL.The distribution of male and female Populus cathayana populations along an altitudinal gradient[J].Acta Ecol Sin,2011,31(23):7067-7074]
10 Grant MC,Mitton JB.Elevational gradients in adult sex ratios and sexual differentiation in vegetative growth rates of Populus tremuloides Michx[J].Evolution,1979,33:914-918
11 Ueno N,Suyama Y,Seiwa K.What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis?[J].J Ecol,2007,95(5):951-959
12 Myers-smith IH,Hikd S.Uniform female-biased sex ratios in alpine willows[J].Am J Bot,2012,99(7):1243-1248
13 Fabbro T,K?rener C.Altit udinal differences in f lower t raits and reproductive allocation[J].Flora-Morphol Distr Funct Ecol Plants,2004,199(1):70-81
14 Guo H,Weiner J,Mazer SJ,Zhao ZG,Du GZ,Li B.Reproductive allometry in Pedicularis species changes with elevation[J].J Ecol,2012,100(2):452-458
15 Zhang L,Luo TX,Liu XS,Wang Y.Altit udinal var iation in leaf construction cost and energy content of Bergenia purpurascens[J].Acta Oecol,2012,43:72-79
16 Lei YB,Chen K,Jiang H,Yu L,Duan BL.Contrasting responses in the growth and energy utilization properties of sympatric Populus and Salix to different altitudes:implications for sexual dimorphism in Salicaceae[J].Physiol Plant,2017,159(1):30-41
17 Cor rens C.The concur rence of male on female ger m cells and the numerical proportion of both genders[J].Naturwissenschaften,1918,6:277-280
18冯毅,王朱涛,蔡应君,任树平,柴成忠,罗建勋.川西北地区康定柳天然群体表型多样性研究[J].西南林学院学院,2010,30:11-20[Feng Y,Wang ZT,Cai YJ,Ren SP,Chai CZ,Luo JX.Study on phenotypic diversity of Salix paraplesia natural populations in northwest Sichuan[J].J SW For Univ,2010,30:11-20]
19李超男,李家宝,李香真.贡嘎山海拔梯度上不同植被类型土壤甲烷氧化菌群落结构及多样性[J].应用生态学报,2017,28(3):805-814[Li CN,Li JB,Li XZ.Soil methanotrophic community structure and diversity in different vegetation types at elevation gradient of Gongga Mountain,Southwest China[J].Chin J Appl Ecol,2017,28(3):805-814]
20 Bing HJ,Wu YH,Zhou J,Sun HY,Luo J,Wang JP,Yu D.Stoichiometric variation of carbon,nitrogen and phosphorus in soils and its implication for nutrient limitation in alpine ecosystem of eastern Tibetan Plateau[J].J Soils Sed,2016,16:405-416
21 Sun H,Wu Y,Yu D,Zhou J.Altitudinal gradient of microbial biomass phosphor us a nd it s relat ionsh ip w it h m icrobial biomass ca rbon,nitrogen,and rhizosphere soil phosphor us on the easter n slope of Gongga Mountain,SW China[J].PLo S ONE,2013,8(9):e72952
22周俊,邴海健,吴艳宏,孙守琴,罗辑.贡嘎山燕子沟土壤磷海拔梯度特征及影响因素[J].山地学报,2016,34(4):385-392[Zhou J,Bing HJ,Wu YH,Sun SQ,Luo J.Variations in soil P biogeochemistry and its impact factors along an altitudinal gradient in the Yanzigou,eastern slope of the Gongga Mountain[J].Mount Res,2016,34(4):385-392]
23徐庆,姜春前,刘世荣,郭泉水.濒危植物四合木种群传粉生态学研究[J].林业科学院研究,2003,16:391-397[Xu Q,Jiang CQ,Liu SR,Guo QS.Study on pollination ecology of endangered plant Tetraena mongolica population[J].For Res,2003,16:391-397]
24 Petzold A,Pfeiffer T,Jansen F,Eusemann P,Schnittler M.Sex ratios and clonal growth in dioecious Populus euphratica Oliv.,Xinjiang Prov.,western China.Trees-Struct Funct,2013,27(3):729-744
25 Che-Castaldo C,Crisafulli CM,Bishop JG,Fagan WF.What causes female bias in the secondary sex ratios of the dioecious woody shrub Salix sitchensis colonizing a primary successional landscape?[J].Am JBot,2015,102(8),1309-1322
26 Obeso J.The costs of reproduction in plants[J].New Phytol,2002,155:321-348
27 Ishida TA,Hattori K,Shibata S,Suzuki M,Kimura MT.Sex allocation of a cosexual wind-pollinated tree,Quercus dentata,in terms of four currencies[J].J Plant Res,2005,118(3):193-197
28李嘉竹,王国安,刘贤赵,韩家懋,刘敏,柳晓娟.贡嘎山东坡C3植物碳同位素组成及C4植物沿海拔高度的变化[J].中国科学D辑:地球科学,2009,39(10):1387-1396[Li JZ,Wang GA,Liu XZ,Han JM,Liu M,Liu XJ.Variations in carbon isotope ratios of C3 plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga[J].Sci China Ser D Earth Sci,2009,39(10):1387-1396]
29 Field DL,Pickup M,Barrett SCH.The influence of pollination intensity on fer tilization success,progeny sex ratio,and f it ness in a windpollinated,dioecious plant[J].Intern J Plant Sci,2012,173(2):184-191
30 Sinclair JP,Emlen J,Freeman DC.Biased sex ratios in plants:theory and trends[J].Bot Rev,2012,78(1):63-86
31 He JD,Dong TF,Huang KC,Yang YX,Li DD,Xu X,He XH.Sexspecific f loral morphology,biomass,and phytohormones associated with altitude in dioecious Populus cathayana populations[J].Ecol Evol,2017,7(11):3976-3986
32 Geraldes A,Hefer CA,Capron A,Kolosova N,Mar tinez-Nu?ez F,Soolanayakanahally RY,Stanton B,Guy RD,Mansfield SD,Douglas CJ,Cronk QCB.Recent Y chromosome divergence despite ancient origin of dioecy in poplars(Populus)[J].Mol Ecol,2015,24(13):3243-3256
33张林静,石云霞,潘晓玲.草本植物繁殖分配与海拔高度的相关分析[J].西北大学学报:自然科学版,2007,37(1):77-80[Zhang LJ,Shi YX,Pan XL.Analysis of correlativity between reproductive allocation and altitude in plants[J].J NW Univ(Nat Sci Ed),2007,37(1):77-90]
34王一峰,刘启茜,裴泽宇,李海燕.青藏高原3种风毛菊属植物的繁殖分配与海拔高度的相关性[J].植物生态学报,2012,36(1):39-46[Wang YF,Liu QQ,Pei ZY,Li HY.Correlation between altitude and reproductive allocation in three Saussurea species on China’s QinghaiTibetan Plateau[J].Chin J Plant Ecol,2012,36(1):39-46]
35樊宝丽,孟金柳,赵志刚,杜国祯.海拔对青藏高原东部毛茛科植物繁殖特征和资源分配的影响[J].西北植物学报,2008,28(4):805-811[Fan BL,Meng JL,Zhao ZG,Du GZ.Influence of altitude on reproductive traits and resource allocation of species of ranunculaceae at East Qinghai Tibetan Plateu[J].Acta Bot Bor-Occid Sin,2008,28(4):805-811]
36苏梅.青藏高原东部高寒草甸九种常见植物叶特征、繁殖特征研究[D].兰州:兰州大学,2009[Su M.Leaf trait and reproductive traits of nine common species of plants at eastern alpine meadow in QinhaiTibetan Plateu[D].Lanzhou:Lanzhou Universtiy,2009]