正如著名生态学家MacArthur(1972)所指出, 科学研究的目的不在于简单地积累事实, 而在于试图发现普遍存在的模式(或规律), 并解释这些模式产生的原因。通过大量的观察和归纳, 在植物繁殖生态学和传粉生物学领域内, 人们已经概括总结了许许多多的模式, 并尝试从机制上予以解释。粗略地讲, 植物繁殖生态学(乃至于任何一门科学)的发展路径主要包括以下几个步骤: 首先对自然现象进行观察描述, 然后从中鉴别出一些规律(即模式); 针对这些模式, 需要给出机理性的解释, 也就是说阐明哪些过程可能会产生这些模式; 最后, 根据已有的模式和其内在过程, 人们可以进行各种预测, 并将预测结果与进一步的观察和实验结果相比较。由于植物繁殖过程受到各种生物与非生物因素的影响, 从不同角度研究同一个问题, 经常会得出矛盾的结论(Mayer et al., 2011)。要从这些千差万别的因素中找出哪个(些)是影响植物繁殖特征的主要选择压力, 或者预测花部特征将如何进化, 是摆在植物繁殖生态学家面前的巨大挑战。
本文的目的就是对植物繁殖生态学和传粉生物学领域内存在的一般模式进行一个初步的总结, 并对导致这些模式的过程(机制)给出可能的答案。虽然具体的生物学细节可能千差万别, 但植物繁殖性状进化的选择压力无外乎两个方面: 要么提高植物通过种子途径获得的雌性适合度(提高种子的数量与质量), 要么提高植物通过花粉途径获得的雄性适合度(成功给胚珠授精)。传统的传粉生物学与植物繁殖生态学研究较多地关注了雌性适合度, 而随着“新植物繁殖生物学”(Morgan & Schoen, 1997)的发展, 人们开始意识到许多植物繁殖性状的进化可能更多地是与提高雄性适合度联系在一起的。从雌雄适合度的综合角度重新审视或综合分析花部适应及植物繁殖效率与成效, 成为当前一个研究热点(黄双全和郭友好, 2000; Ashman, 2002; Sun et al., 2008; Mao & Huang, 2009)。
1 为什么绝大多数植物都是雌雄同体的?
自然界大约72%的植物物种都产生两性花, 如果包括雌雄同株(monoecy)、雄全同株(androm- onoecy)、雌全同株(gynomonoecy)在内, 雌雄同体约占被子植物物种数的90%左右(Yampolsky & Yampolsky, 1922)。或者说, 雌雄功能结合在同一个植株内, 是植物的一个普遍模式。以前人们对这个模式的解释都是归因于雌雄同体(尤其是两性花)的自交繁殖保障优势、广告优势(花与花序可以吸引传粉者, 既为雌蕊带来花粉实现雌性适合度, 又能把花粉带出实现雄性适合度), 但以Charnov(1982)为代表的现代观点则认为, 从资源分配的角度能够更好地解释雌雄同体为何有如此高的普遍性。
由于雌雄两种性别功能同时存在于花内或植株上, 雌雄同体植物的资源分配包括了2个方面: 繁殖资源的投入(reproductive investment)和两性功能的分配(sex allocation)(Zhang, 2006)。在大多数情况下, 受到植株大小与环境条件的限制, 繁殖资源投入的增加所导致的适合度回报很快达到极限。尤其是受到传粉昆虫体型与梳理(grooming)行为的限定, 花粉量的增加通常并不能相应地提高花粉输出率, 传粉者的每次访问只能将大约1%左右的花粉移至可授柱头(Harder, 2000), 雄性适合度与资源投入之间一般呈现出投入回报率递减的规律(Charnov, 1982; Campbell, 2000)。根据性别分配理论, 某个性别投入的资源与适合度收益之间的关系决定了是否雌雄同体: 如果适合度回报率随着资源投入增加而减少, 雌雄同体将是植物更有效地利用资源从而实现总适合度(雌性+雄性)最大化的一种策略(Charnov, 1982), 这是可被自然选择保留的进化稳定对策(Charnov, 1982; Campbell, 2000; 张大勇和姜新华, 2001)。除前面提及的繁殖保障优势与广告优势外, 其他一些因素, 如花粉与种子生产分别利用不同的资源、雌雄功能资源需求时间的差异(即雌雄异熟, dichogamy)可能会使得雌雄同体更加稳定, 但不大可能是造成雌雄同体的主导因素(Charnov, 1982; 张大勇和姜新华, 2001; Zhang, 2006)。
与虫媒传粉植物不同, 风媒传粉的植物一般不存在雄性适合度的增加随着资源投入而很快达到饱和的现象(如同等风力条件下花粉的增多将直接增加花粉输出率), 使得雌雄同体的稳定性下降, 而雌雄异株可能将在选择上具优势。风媒传粉与单性花、雌雄异株的这种相关性已被广为认可(Charlesworth, 1993; Renner & Ricklefs, 1995), 从另一方面进一步证实了资源分配格局是决定花的性别与交配系统的关键因素。
从上面的分析中我们注意到, 雄性功能的资源分配和雄性适合度的实现是塑造花部特征的重要因素(Sutherland & Delph, 1984), 因此我们需要更加重视两性花的雄性功能及其在花部特征塑造与花进化上的贡献。另一方面, 从雄性适合度角度出发, 也将更有助于人们加深对花部特征、繁殖策略与资源分配关系的理解。实际上, 早在达尔文时代的植物学家就非常重视两性花的雄性适合度。达尔文本人就认为雌雄异位(herkogamy)与异型花柱(heterostyly)等花部特征主要是在促进花粉散发、降低雌蕊对雄蕊散粉影响的选择压力下发生与维持的(Darwin, 1877; Webb & Llyod, 1986; 任明迅和张大勇, 2004), 而自交的避免可能只在部分植物中作为主要选择压力出现, 在更多的时候可能只是一个“副产品”。Muchhala等(2010)甚至认为, 简单地提高雄性适合度的选择就足以导致传粉系统的转变, 即在传粉者访问率足够高、能移走花药内大部分花粉的情况下, 花将依赖专化传粉者以降低花粉被带到其他物种的几率, 提高雄性适合度, 最终结果是花部特征与传粉系统发生特化; 而在传粉者访问率较低的情况下, 传粉系统将发生泛化, 以便更多的传粉者移走花药内的花粉。近年来, 越来越多的研究也证实了雄性适合度在塑造花部特征与传粉系统方面的重要作用(Barrett, 2002; Muchhala et al., 2010; Weigend et al., 2010; Dai & Galloway, 2011)。
2 为什么大多数植物都是先开花、后结果?
虽然先开花、后结果是一个当然的顺序, 但在植株水平上花果期是可以重叠的, 即所谓的“边花边果”。然而, 大多数植物在开花之后都有相当长的果实成熟期, 或者说, 不仅在单花水平上而且在整个植株水平上, 花果期存在很大程度的分离。以往几乎所有的性别分配模型都把雌雄同体植物花果期的这种分离, 即雌雄功能的时间更替, 归结为外部因素的制约(Charlesworth & Charlesworth, 1987; Sato, 2000, 2004)。如Westoby和Rice(1982)认为, 为了避免在未能成功受精的(或者遗传质量低的)胚珠上浪费资源, 植物在对受精胚珠进行筛选之后才开始对后代进行资源投入; Day和Aarssen(1997)也认为, 可能仅仅是因为结实与坐果行为的启动与完成需要更长的时间, 才导致花期后要经历一段时间才会完成结实与坐果这一雌性功能。
然而, 花果期的分离也可能是一个适应性状。Zhang(2006)通过一个简单的模型发现, 花果期的分离可以作为植株应对资源水平随机波动的一个适应机制, 并非完全是受到外界因素影响的后果。具体而言, 在不同资源水平下, 雌雄功能的收益是不同的。如果我们假设花期资源投入为雄性投入, 而且雌性适合度是资源的线性函数, 那么只有当资源水平达到一个临界值时(即雄性和雌性资源投入的边际回报率相等时), 即雄性功能收益开始小于雌性功能的时候, 植株才会将资源转到雌性功能上, 即开始结实与坐果(Zhang, 2006)。当然, 这种从雄到雌的“开关”转换只有在雌性适合度为线性函数时才可能发生; 如果雌性适合度不是线性的但也是饱和增加的(但饱和速率通常低于雄性适合度函数), 那么从雄到雌的转换将是逐渐的, 植株的雌雄功能将会重叠一段时间; 如果雄性适合度是资源投入的一个S型曲线(或者与个体大小直接相关, 例如风媒植物, 其较小个体的花粉扩散可能非常受限), 那么繁殖投入甚至可能会表现为从雌到雄再到雌的转换(Zhang, 2006)。
支持Zhang(2006)理论模型的实验证据目前虽然还很少, 但Friedman和Barrett(2011)关于普通豚草(Ambrosia artemisiifolia)的研究提供了一个可能的实例。该研究发现, 在正常光照和遮荫条件下, 豚草植株表现出了不同的雌雄资源分配策略和时间节律, 与上述理论模型的预期一致。不过, 在考虑花果期分离的这种主动适应机制的同时, 我们也应注意到Westoby和Rice(1982)、Day和Aarssen (1997)以及Sato(2000, 2004)提及的发育限制与母体选择等因素的作用, 它们可能也是影响花果期是否分离以及分离时间长短的重要因素, 这都有待于将来进一步的工作来证实。
3 为什么植物大量开花而结实率却很低?
植物的结实率与坐果率通常都很低(Burd, 1998), 坐果率最低不到1%, 结实率可低至5%。结实率最高的类群是一年生植物, 但一般也只是在80-90%左右; 甚至一些闭花受精的一年生植物(如春小麦), 其结实率也仅有85%左右(段舜山等, 1995)。可见, 植物的结实率普遍达不到100%的主要原因不太可能是花粉限制。
Wilson和Rathcke(1974)针对这一问题开展了开创性的工作。他们认为两性花结实率偏低的一个主要原因是那些未能结实的“多余”的花可能扮演着向外散粉的雄性角色, 这是植株竞争雄性繁殖机会而导致的一个后果。Sutherland和Delph(1984)对比了文献中报道的316个两性花物种和129个雌雄同株或雌雄异株物种的结实率, 发现两性花物种普遍比后两类物种的结实率要低, 这一结果证实了Wilson和Rathcke(1974)的结论。但是, 如果这些“多余的”花真的只是执行雄性功能, 这些花就应该进化为完全的雄花, 即大部分植物应该进化成雄花-两性花同株(雄全同株)的性系统。然而, 实际上雄全同株仅占被子植物的3%左右(Yampolsky & Yampolsky, 1922), 远不如两性花(约70%)那么普遍。这说明, 这些“多余的”两性花中的雌蕊可能也具有适应意义。
Burd(1998)指出, “多余的”花可能通过以下途径促进雌性适合度: (1)“多余的”花形成较大的花序, 吸引更多的传粉者, 使得柱头落置更多花粉; (2)“多余的”花可能在不可预期的、偶尔发生的资源或传粉充足的条件下提高结实率; (3)在啃食者、不利气候或机械损伤等造成胚珠损失的情况下, “多余的”花可能提供一定的繁殖保障; (4)“多余的”花可能为植株提供了更广泛的选择余地, 可以对受精更好的胚珠选择性地投入资源和选择性地结实。Burd (1998)通过模型研究证实了较低的结实率可能是因为植物选择性结实的后果。可见, 植物产生 “多余的”花虽然没有直接提高结实率, 但可以通过对质量较好的果实选择性投入资源(将质量不好的果实流产)而间接提高雌性适合度。显然, 这种策略主要在交配环境多变、果实质量差异较大的环境中被选择(Burd, 1998), 而在差异不显著的果实中进行此类选择所获得的收益非常有限。
结实率较低往往意味着开花数量较多, 但这些花可以是渐次开放的, 也可能是同时大量开放。Bawa(1983)指出, 这可能与果实生产的资源可获得性有关: 与大量同时开花相比, 渐次开花使得植株可以更灵活地控制花、果之间的资源分配。而且, 同时大量开花也可能造成同株异花授粉(geitonogamy)增加, 导致雌性与雄性适合度的下降(Harder & Barrett, 1995)。但是, 同时大量开花在相当多的物种中出现, 说明它可能具有适应意义。Schoen和Dubuc (1990)的模型研究表明, 如果花序增大使得其中每朵花的花粉贡献也增大, 那么大花序将会被选择, 植株就会大量同时开花。换句话说, 大量同时开花可以通过提高对昆虫的吸引力来提高植株的花粉输出, 从而提高雄性适合度。另一方面, 由于大多数花内的雌蕊与雄蕊的成熟时间不同(dichogamy, 雌雄异熟), 在一个很短的时间内大量开花意味着雌雄功能在时间上很少重叠, 可降低同株异花授粉的风险(Harder & Barrett, 1995), 而渐次开花反而会使雌雄功能重叠程度增大(Zhang, 2006); 再加上花序内的花往往有着一定的功能分化(见第6节), 同时开花可进一步降低同株异花授粉的可能性。基于上述原因, 大量同时开花存在于很多植物中, 在部分植物中由于不完全的雌雄异熟可能造成的同株异花授粉也许是大量同时开花在促进异交花粉输出时无法避免的一个后果(张大勇和姜新华, 2001)。或者说, 同时大量开花尽管可能在某种程度上伤害了雌性适合度, 但显著地提高了雄性适合度, 只要雄性适合度的增加量大于雌性适合度的减少量, 那么它就仍然是一个适应性状。
4 为什么在胁迫生境中植物倾向于具有异交的繁育系统?
达尔文最早注意到异交的繁育系统(如雌雄异株、雌全异株、自交不亲和等)更倾向于出现在干旱或者其他胁迫生境中(Delph, 2003)。例如在伊比利亚半岛, 葫芦科植物喷瓜(Ecballium elaterium)的性系统存在着地理分化, 雌雄异花同株的亚种出现在北部湿润地区, 而雌雄异株的亚种出现在南部干旱地区(Costich, 1995)。在许多雌全异株的物种中, 随着环境胁迫的增强, 雌株在种群内所占比例越来越大, 而两性花个体生产的果实却越来越少, 这就显著降低了自交产生后代的可能性(Delph, 2003)。然而, 环境胁迫与异交繁育系统正相关的这样一个模式并不符合人们的直觉, 因为通常情况下, 环境胁迫会导致植物的密度较低或者传粉者减少, 此时自交就更有可能成为繁殖的保障。
研究发现, 胁迫环境中的两性花个体一般倾向于把更多资源分配给雄性功能(Charnov, 1982; Lloyd & Bawa, 1984; 张大勇, 2004)。具体而言, 胁迫生境中可利用资源总量的差异导致了不同形式的适合度收益曲线; 由于环境胁迫很可能意味着个体在繁殖上投入的资源减少, 雄性适合度收益可能趋于线性甚至加速递增, 而雌性适合度收益如果是线性的则不受资源总量的影响。这使得单性花或单性个体在胁迫环境中比两性花具有相对更高的雌性适合度, 有利于单性花和异交的进化维持(Delph, 1990a, b; 张大勇, 2004)。另外, 有研究发现, 胁迫生境往往加剧植物的近交衰退(Dudash, 1990; Cheptou et al., 2000), 这显然会进一步促进异交繁育系统的选择(Dudash, 1990)。
不仅物理胁迫, 生物胁迫也可能导致单性花和异交的产生。Ashman(2002)研究发现, 植食动物往往更多地取食产生花粉的个体, 这既有利于雌花和雌株的出现与扩散, 也有利于此类个体改变资源分配的模式, 促进了两性花个体通过雌全同株向雌雄异株进化, 单性花和异交交配系统也由此得以产生和维持。
但是也有研究发现, 胁迫生境造成的传粉条件与传粉质量的下降, 可能导致自交率上升(Schoen & Brown, 1991)。但严酷的高山环境是一个反例: 虽然访花昆虫访花频率下降, 但大多数植物仍以异交繁育系统(雌雄异株和自交不亲和等)为主(Arroyo et al., 1985)。究其原因, Arroyo等(1985)认为, 植物可以通过增加对花朵的资源投入, 用更鲜艳的颜色、更浓的花蜜等来吸引访花昆虫, 而非通过自交来适应传粉昆虫数量的下降。但是, 到底哪些植物会在胁迫生境中以自交来应对逆境, 哪些植物是以强化异交成功率来适应不良生境?人们还没有找到其中的规律。
5 为什么一年生植物往往倾向于自交?
Barrett等(1996)通过重建花荵科交配系统与生活史性状的进化历史, 以及比较系统发育有效种对后发现, 一年生物种往往具有较高的自交率, 多年生物种尤其是木本植物的自交率则很低。由于一年生植物生活史短、繁殖期短, 繁殖成功率难以保障, 很早就有人提出其较高的自交率可能是繁殖保障的结果。但是, Morgan和Schoen(1997)的模型研究结果显示, 多年生植物个体由于反复繁殖, 近交衰退效应持续累积, 降低了个体的存活力与繁殖能力。另一方面, 由于多年生植物存在较高的突变负荷, 加剧了近交衰退, 导致自交的多年生植物比一年生植物付出更多的适合度代价(Morgan & Schoen, 1997; 张大勇和姜新华, 2001; 张大勇, 2004)。因此, 可能是自交使多年生植物付出更多的代价, 而不是自交给一年生植物带来的繁殖保障, 造成了一年生植物有较高的自交率, 而多年生植物有较高的异交率。
同样是通过模型研究, Zhang(2000)发现, 不仅植物的生活史会影响交配系统, 交配系统也可反过来通过调整资源分配格局来改变生活史。在自交能够进化的条件下(即近交衰退较弱), 自交率将在自然选择的作用下不断增加, 这将促使植物把越来越多的资源分配给繁殖功能, 而植株存活到下一年的概率则因此越来越低。极端情形下, 自交甚至会改变植物的生活史, 使之从多年生转变为一年生。但是, 到目前为止还没有任何证据支持自交率与繁殖分配的这种正相关关系(Zhang, 2000)。
6 为什么许多植物同一花序内的花会产生形态与功能上的分化?
由于在花序上的空间位置以及开花时间不同, 同一花序的花往往具有不同的大小、形态与结构(Buide, 2008; Tang & Ren, 2011)。这些花可能具有不同的资源分配格局、不同的访花昆虫访问频率, 造成花粉数、胚珠数、花粉输出与落置等方面的不同(Buide, 2008)。Tang和Ren(2011)在芸香(Ruta graveolens)中发现, 同一个花序上位于顶端的花较早开放, 且为花瓣5、雄蕊10的五数花; 而位于花序其他部位的花均为花瓣4、雄蕊8的四数花。与四数花相比, 五数花的胚珠数更多、子房更大, 因而资源分配偏向雌性; 不仅如此, 五数花的结实率更高, 在功能上也更偏向雌性。晚开的四数花则具有较高的花粉输出率, 在功能上偏向雄性。因此, 芸香花序不同部位的花在资源分配与性别功能上发生了相对应的分化(Tang & Ren, 2011)。
同一花序内不同位置的花甚至可能在性别分配上发生分化, 导致花具有不同的性别。雄花-两性花同株(即雄全同株)是目前研究花序内花性别分化和资源分配等较集中的一个模式系统。Liao和Zhang(2008)发现, 藜芦(Veratrum nigrum)位于顶生花序(两性花)下方的雄花在避免花粉贴现(pollen discounting)的同时增强了对传粉者的吸引, 从而提高了两性适合度。Zhang和Tan(2009)也认为, 新疆干旱区低矮灌木刺山柑(Capparis spinosa)雄全同株的雄花节约了生产雌蕊的资源, 主要是为了吸引传粉者和实现雄性适合度。在热带草质藤本粉色西番莲(Passiflora incarnata)中, Dai和Galloway(2012)证实雄花的主要适应意义在于提高了雄性适合度, 同时还避免了在雌性功能上的资源浪费。喜树(Camptotheca acuminata)的雄全同株表现为聚伞花序, 上方的伞形花序均为两性花, 而最下方的一二个花序由雄花组成; 上方两性花通常早开、花更大, 下方的雄花则较小(徐申林和刘文哲, 2011)。
以上研究结果都证实, 花序内花分化的基本趋势表现为: 位于上方的早开花资源更丰富、功能更偏雌性, 下方后开的花功能偏雄, 甚至完全转变为雄花。根据最优资源分配假说, 雄全同株只有在果实生产代价较大且最优雄花数多于能结实的花数时才会出现; 一旦果实生产实现的雌性适合度接近饱和, 在雌性功能上继续投入的收益将急剧减少, 产生只具有雄性功能的花将是一种节约资源实现收益最大化的繁殖策略(Bertin, 1982; 廖万金等, 2003)。
与上述植物不同, 一年生水生植物冠果草(Sagittaria guyanensis ssp. lappula)的总状花序中, 先开的两性花位于下方, 后开的雄花位于上方。研究发现, 雄花极少有昆虫访问, 因此很难实现雄性繁殖适合度(Huang et al., 2000; Huang, 2003)。冠果草是慈姑属中少数雄全同株的物种, 该属其余物种都是多年生雌雄同株或雌雄异株的(Huang, 2003)。因此, 与其他植物的雄全同株不同, 冠果草中的两性花可能是从单性的雌花次生而来。Huang(2003)的实验研究发现, 冠果草雄全同株的两性花具有花内自交的繁殖保障潜能, 与同属的雌雄同株和雌雄异株相比, 更能适应花粉限制环境(Huang et al., 2000; Huang, 2003)。前面已经提到, 花内自交(导致自交率上升)与一年生习性可以互为因果, 是繁殖资源的投入与性别功能分配权衡的结果(Zhang, 2000, 2006)。因此, 冠果草的雄花在花序上的位置及其繁殖功能有别于其他雄全同株物种的可能原因是其一年生的生活史以及特殊的进化历史。可见, 在研究雄全同株以及其他类似性系统的时候, 需要同时考虑该物种的进化历史和资源分配格局。
花序内更为极端的花分化是伞形花序中经常出现的位于边缘的不育花, 如绣球花科(或虎耳草科绣球花属)和忍冬科(或五福花科)荚蒾属(Jin et al., 2010)。这些不育花完全丧失了直接繁殖的功能(雌蕊与雄蕊均退化), 但凭借其花瓣(通常比花序中央的可育花的花瓣更大)吸引传粉者, 如绣球(Hydrangea macrophylla)、绣球荚蒾(Viburnum macrocephalum)(Jin et al., 2010)。从资源分配的角度来看, 伞形花序边缘的花可能很难受到传粉者的直接访问, 因此其很低的花粉输出与柱头花粉落置就导致了资源分配由雌雄蕊转向吸引器官如花瓣; 同时, 处于花序中央的花则降低了在花瓣上的资源投入甚至花瓣完全消失。这就使得繁殖资源在花序水平进行了再分配, 边缘花通过较大的花瓣维持了伞形花序的大小和形状, 维持甚至提高了花序对传粉者的吸引(Jin et al., 2010)。
菊科植物头状花序的边花与盘花的资源分配格局也可能显著不同, 从而导致头状花序不同位置的花大小与功能均不相同。很多菊科植物的头状花序的边花是花瓣长而特化的舌状花(雌花)、中央的盘花则是花瓣严重退化的筒状花(两性花)。与上述伞形花序类似, 菊科头状花序中的这种花分化(雌花、两性花同株)可能是繁殖资源在繁殖器官与吸引器官之间的分配策略不同造成的。更特别的是, 巨菊属(Pyrethrum)头状花序边花的舌状花瓣在夜间或寒冷的雨天向内翻卷, 包住盘花, 而且边花的化学防御物质比中央的盘花约多1/3(Darwin, 1877)。这表明一些菊科植物头状花序的边花可能具有保护与防御功能, 这种分化需要用生长-繁殖-防御之间的资源分配来解释。另一方面, 由于伞形花序与头状花序都由非常多的花组成, 花粉容易在花序内不同花之间散布, 即同株异花传粉, 导致向外输出的异交花粉量降低。因此, 花序的大小与数量将由花的资源量、自交率、结实率以及花粉输出之间的功能关系决定(Schoen & Duhuc, 1990; 张大勇和姜新华, 2001)。
7 为什么两性花会产生异型雄蕊?
大多数两性花只有一个或少数几个雌蕊, 而雄蕊数量众多。这些数量众多的雄蕊可能在花内资源分配调整下发生分化。特化的传粉系统往往伴随着花内雄蕊数量的明显减少(Vogel, 1978)。在以花粉为回报物的花中, 为数不多的花药与花粉面临着被传粉者取食或参与正常繁殖的两难境地(Vallejo-Marín et al., 2009, 2010)。这种情况下, 花往往会调整资源分配模式, 发展出“异型雄蕊”(heteranthery)来确保有足够的花粉实现繁殖(Vogel, 1978; Luo et al., 2008)。狭义的异型雄蕊是指花内部分雄蕊的花药特化成专门吸引传粉者、花粉活性或繁殖能力很低的“喂食型花药”(feeding anthers), 另一部分雄蕊的花药则是“传粉型花药”(pollinating anthers), 保留着正常的繁殖潜力(Darwin, 1877; Luo et al., 2008; Vallejo-Marín et al., 2009, 2010)。异型雄蕊得以发生与维持的主要原因可能是, 在资源限制条件下, 一部分花药放弃繁殖功能而使资源集中在少数花药与花粉上, 以获得更高的雄性适合度(Vallejo-Marín et al., 2009, 2010)。
在鸭跖草科中, 雄蕊还发生了更为复杂的三型分化(Ushimaru et al., 2003)。如雄全同株的鸭跖草(Commelina communis), 雄花和两性花中都具有3类雄蕊: 2个长雄蕊、1个中长雄蕊、3个短雄蕊。长雄蕊的花粉数远多于中长雄蕊, 而短雄蕊仅产生少量不育的花粉。雄蕊的这种三型分化伴随着雄蕊大小与形态、花粉数量与活性的变化, 显然与上述两型分化的异型雄蕊一样, 都是资源分配与功能分化的结果。Ushimaru等(2003)研究发现, 长雄蕊的花粉主要参与异交传粉, 中长雄蕊的花粉给传粉者提供回报物, 而短雄蕊可能主要是通过夸张变形的花药产生的极少量的不育花粉来吸引传粉者。花内雄蕊的这种三型分化, 也许是花内水平能达到的最为复杂多样的资源分配格局。
花内的雄蕊不仅在花药形态和花粉活性上存在着分化, 往往还在花药开裂与花粉成熟时间等方面也存在分化, 体现出一种“花粉分发”(pollen dispensing)策略(Harder & Wilson, 1994): 在传粉昆虫访问频率较高的情况下, 植物将花粉包装和分发在不同的空间与时间上, 通过不同传粉昆虫分批、逐次散粉, 以将花粉输出率最大化。雄蕊的这种分化有时还伴随着雄蕊的不同步运动(Weigend et al., 2010; 任明迅, 2010)。Weigend等(2010)发现, 访花昆虫可诱导刺莲花科的雄蕊分批、逐次向花内运动, 从而造成雄蕊在空间位置、花粉成熟与散粉时间上的分化。Tang和Ren(2011)在芸香中也发现了同样的现象。花内雄蕊的这一特性被认为是花实现资源节约和繁殖最大化的一种适应结果(Weigend et al., 2010; Tang & Ren, 2011), 可以看成是花粉分发机制的一种特殊方式(任明迅, 2010), 反映了花内资源分配的极大可塑性。
8 结语
本文从自然选择和适应角度阐释了植物繁殖性状的进化问题, 但同时需要强调的是, 并非所有的性状都一定具有适应意义。例如, 雌雄同体植物往往都表现出一定程度的自交(Goodwillie et al., 2005)。虽然自交可能具有各式各样的适应意义, 但现有的证据表明, 多年生植物的自交后代基本上都不能存活到成熟期, 说明这类自交并非适应的, 而更有可能是大量花同时开放而无法避免的一个后果(Barrett, 2003)。
花部特征和繁殖策略是在外界生物与非生物因素影响下, 由植株、花序以及花不同水平的资源分配格局决定的(Charlesworth & Charlesworth, 1987; Charnov, 1982; Zhang, 2000, 2006)。正如张大勇(2004)所言, 植物的繁殖性状是植物资源投入-收益长期权衡的后果。生态学之所以被称为“自然的经济学”, 原因之一在于它将资源投入与分配及其收益之间的权衡作为理解自然界各种生物学特征及适应进化的基础。花的形态结构、性别与功能、交配系统等既是个体适合度最大化的长期选择的结果, 也受限于进化历史和发育与生理等因子。我们可能要习惯于接受这样一个观点: 花, 是植物个体在长期进化历史中各个选择力量博弈、妥协的一个后果。
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[本文引用: 1]
Sodium (Na) has a unique role in food webs as a nutrient primarily limiting for plant consumers, but not other trophic levels. Environmental Na levels vary with proximity to coasts, local geomorphology, climate, and with anthropogenic inputs (e.g., road salt). We tested two key predictions across 54 grasslands in North America: Na shortfall commonly limits herbivore abundance, and the magnitude of this limitation varies inversely with environmental Na supplies. We tested them with a distributed pulse experiment and evaluated the relative importance of Na limitation to other classic drivers of climate, macronutrient levels, and plant productivity. Herbivore abundance increased by 45% with Na addition. Moreover, the magnitude of increase on Na addition plots decreased with increasing levels of plant Na, indicating Na satiation at sites with high Na concentrations in plant tissue. Our results demonstrate that invertebrate primary consumers are often Na limited and track local Na availability, with implications for the geography of invertebrate abundance and herbivory.
Pollen resistance to water in 80 angiosperm species: flower structures protect rain susceptible pollen
DOI:10.1111/nph.2009.183.issue-3 URL [本文引用: 1]
Pollination ecology in the 21st century: key questions for future research
DOI:10.26786/1920-7603 URL [本文引用: 1]
The role of theory in an emerging new plant reproductive biology
DOI:10.1016/s0169-5347(97)01045-8
URL
PMID:21238055
[本文引用: 3]
Recent empirical studies hint at an end to the historical solitude between pollination and mating system approaches to plant reproductive character evolution. Now is an opportune time to distill theoretical results into comprehensible insight, and to integrate these findings into the emerging new plant reproductive biology. We outline four theoretical insights for understanding the evolution of reproductive characters, and show how these allow researchers to dissect complex ecological scenarios into clear and evolutionarily relevant components.
Competition drives specialization in pollination systems through costs to male fitness
DOI:10.1086/657049
URL
PMID:20954889
[本文引用: 2]
Specialization in pollination systems played a central role in angiosperm diversification, yet the evolution of specialization remains poorly understood. Competition through interspecific pollen transfer may select for specialization through costs to male fitness (pollen lost to heterospecific flowers) or female fitness (heterospecific pollen deposited on stigmas). Previous theoretical treatments of pollination focused solely on seed set, thus overlooking male fitness. Here we use individual-based models that explicitly track pollen fates to explore how competition affects the evolution of specialization. Results show that plants specialize on different pollinators when visit rates are high enough to remove most pollen from anthers; this increases male fitness by minimizing pollen loss to foreign flowers. At low visitation, plants generalize, which minimizes pollen left undispersed in anthers. A model variant in which plants can also evolve differences in sex allocation (pollen/ovule production) produces similar patterns of specialization. At low visitation, plants generalize and allocate more to female function. At high visitation, plants specialize and allocate equally to both sexes (in line with sex-allocation theory). This study demonstrates that floral specialization can be driven by selection through male function alone and more generally highlights the importance of community context in the ecology and evolution of pollination systems.
Stamen movements in hermaphroditic flowers: diversity and adaptive significance
Herkogamy
In: Plant Life-History Evolution and Reproductive Ecology (植物生活史进化与繁殖生态学) (ed. Zhang DY (张大勇)), pp. 310-331. Science Press, Beijing. (in Chinese)
Dioecy and its correlates in the flowering plants
Effects of phenological constraints on sex allo- cation in cosexual monocarpic plants
Size-dependent sex allocation in hermaphroditic plants: the effects of resource pool and self-incompatibility
DOI:10.1016/j.jtbi.2003.11.006
URL
PMID:14990390
[本文引用: 2]
The effects of the resource pool and resource obtained during a season for seed maturation and self-incompatibility on the size-dependency of evolutionarily stable sex allocation were analysed theoretically. In hermaphroditic plants, reproductive resources allocated between male and female function may not be paid from a single resource pool, because plants can mature seeds using not only reserved resources but also newly gained resources after flowering. But the resource investment to male function is limited to the flowering stage. Under the assumption of constant reserve efficiency and diminishing resource return per investment to leaves, large plants should use both reserved and newly gained resources for seed maturation, while small plants should use only new resources. When both reserved and new resources are used, the optimal allocation for self-compatible species is to invest a constant amount of resources into male function irrespective of resource size, because the female fitness curve increases linearly and the male curve decelerates due to local mate competition. In self-incompatible species, on the other hand, fitness gain per investment through male function and the optimal amount of resources invested in male function decrease with size. Thus a decrease in maleness with size should be emphasized more in self-incompatible species than in self-compatible one. When only new resources are used for seed growth, the female fitness curve as well as male one decelerates with investment. Consequently, the investment in both male and female functions should increase with size, in both self-compatible and self-incompatible species. The magnitude of reserve efficiency relative to efficiency of resource gain after flowering affects size-dependent pattern of sex allocation, while the cost of seed maturation relative to ovule production has little effect on it. The plant size variation in a population emphasizes size-dependency of sex allocation. When size variation is large enough, it is possible that large plants become complete female in self-incompatible species, but it is not in self-compatible species.
Whole- and within flower self-pollination in Glycine argyrea and G. clandestina and the evolution of autogamy
DOI:10.1111/j.1558-5646.1991.tb02670.x
URL
PMID:28564133
[本文引用: 1]
The overall rate of self-fertilization can be viewed as the sum of two distinct processes: 1) self-pollination of all ovules in a flower (whole-flower self-pollination); and 2) self-pollination of some of the ovules in a flower, occurring together with outcrossing of the remaining ovules (part-flower self-pollination). In some situations these processes may be equated with different modes of self-pollination. A model of the mating system in which the progeny of separate fruits serve as the unit of observation is presented. The model partitions the overall rate of self-pollination into components attributable to whole- and part-flower selfing. When the mating system is estimated using information on marker genotypes from chasmogamous fruits in two species of Glycine together with the whole- and part-flower selfing model, the results indicate that the chasmogamous flowers in a subalpine population of G. clandestina underwent a significant level of whole-flower selfing, whereas in another, lower elevation population of G. clandestina and in a subtropical population of G. argyrea, they did not. This difference is thought to be related to the contrast in the variability of environmental conditions for insect-mediated pollination between the habitats sampled. In particular, the large component of whole-flower selfing observed in the subalpine population of G. clandestina may be due to self-pollination that is induced during periods unfavorable to insect-mediated pollination. It can be demonstrated that such induced selfing will be selected whenever environmental conditions are such that pollinator activity limits seed set, and moreover that induced selfing can result in the selection of overall levels of self-pollination that are intermediate between 0 and 1. Monte Carlo simulation is employed to show that ignoring the correlation of self-fertilization events that result from whole- and part-flower selfing may lead to biased estimates of mating system parameters.
The evolution of inflorescence size and number: a gamete-packaging strategy in plants
Multif- unctional bracts in the dove tree Davidia involucrata (Nys- saceae: Cornales): rain protection and pollinator attraction
DOI:10.1086/523953
URL
PMID:18171156
[本文引用: 1]
Although there has been much experimental work on floral traits that are under selection from mutualists and antagonists, selection by abiotic environmental factors on flowers has been largely ignored. Here we test whether pollen susceptibility to rain damage could have played a role in the evolution of the reproductive architecture of Davidia involucrata, an endemic in the mountains of western China. Flowers in this tree species lack a perianth and are arranged in capitula surrounded by large (up to 10 cm x 5 cm) bracts that at anthesis turn from green to white, losing their photosynthetic capability. Flowers are nectarless, and pollen grains are presented on the recurved anther walls for 5-7 days. Flower visitors, and likely pollinators, were mainly pollen-collecting bees from the genera Apis, Xylocopa, Halictus, and Lasioglossum. Capitula with natural or white paper bracts attracted significantly more bees per hour than capitula that had their bracts removed or replaced by green paper. Experimental immersion of pollen grains in water resulted in rapid loss of viability, and capitula with bracts lost less pollen to rain than did capitula that had their bracts removed, suggesting that the bracts protect the pollen from rain damage as well as attracting pollinators.
On the importance of male fitness in plants: patterns of fruit-set
DOI:10.2307/1938317 URL [本文引用: 2]
Sex allocation and functional bias of quaternary and quinary flowers on same inflorescence in the hermaphrodite Ruta graveolens
DOI:10.1016/j.actao.2011.05.013 URL [本文引用: 5]
Evidence for reductions in floral attractants with increased selfing rates in two heterandrous species
Variation in floral organ size depends on function: a test with Commelina communis, an andromonoecious species
Trait correlates and functional significance of heteranthery in flowering plants
Division of labour within flowers: heteranthery, a floral strategy to reconcile contrasting pollen fates
DOI:10.1111/j.1420-9101.2009.01693.x
URL
PMID:19320798
[本文引用: 3]
In many nectarless flowering plants, pollen serves as both the carrier of male gametes and as food for pollinators. This can generate an evolutionary conflict if the use of pollen as food by pollinators reduces the number of gametes available for cross-fertilization. Heteranthery, the production of two or more stamen types by individual flowers reduces this conflict by allowing different stamens to specialize in 'pollinating' and 'feeding' functions. We used experimental studies of Solanum rostratum (Solanaceae) and theoretical models to investigate this 'division of labour' hypothesis. Flight cage experiments with pollinating bumble bees (Bombus impatiens) demonstrated that although feeding anthers are preferentially manipulated by bees, pollinating anthers export more pollen to other flowers. Evolutionary stability analysis of a model of pollination by pollen consumers indicated that heteranthery evolves when bees consume more pollen than should optimally be exchanged for visitation services, particularly when pollinators adjust their visitation according to the amount of pollen collected.
Evolutionary shifts from reward to deception in pollen flower
In: The Pollination of Flowers by Insects (ed. Richards AJ), pp. 89-96. Academic Press. London.
The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy
Reloading the revolver-male fitness as a simple explanation for complex reward partitioning in Nasa macrothyrsa (Loasaceae, Cornales)
DOI:10.1111/j.1095-8312.2010.01419.x URL [本文引用: 4]
Evolution of seed plants and inclusive fitness of plant tissues
DOI:10.1111/j.1558-5646.1982.tb05437.x URL PMID:28568226 [本文引用: 1]
Adaptive design of the floral display in Asclepias syriaca L
Intra-inflorescence sex expression and allocation in Camptotheca acuminata
DOI:10.3724/SP.J.1258.2011.01290 URL [本文引用: 1]
Distribution of sex forms in the phanerogamic flora
Resource allocation and the evolution of self-fertilization in plants
DOI:10.1086/303310
URL
PMID:10686160
[本文引用: 4]
This article develops a simple evolutionarily stable strategy (ESS) model of resource allocation in partially selfing plants, which incorporates reproductive and sex allocation into a single framework. The analysis shows that, if female fitness gain increases linearly with resource investment, total reproductive allocation is not affected by sex allocation, defined as the fraction of reproductive resources allocated to male function. All else being equal, the ESS total reproductive allocation increases with increasing selfing rate if the fitness of selfed progeny is more than half that of outcrossed progeny, while the ESS sex allocation is always a decreasing function of the selfing rate. Self-fertilization is much more common in annual than in perennial plants, and this association has been commonly interpreted in terms of an effect of life history on mating system. The model in this article shows that self-fertilization can itself cause the evolution of the annual habit. Incorporating the effects of pollen discounting may not have any influence on total reproductive allocation if female fitness gain is a linear function of resource investment, although the evolutionarily stable sex allocation is altered. Evolution of the selfing rate is found to be independent of reproductive and sex allocation under the mass-action assumption that self- and outcross pollen are deposited simultaneously on receptive stigmas and compete for access to ovules.
Evolutionarily stable reproductive inves- tment and sex allocation in plants
In: Ecology and Evolu- tion of Flowers (eds Harder L, Barrett SCH), pp. 41-60. Oxford University Press, Oxford.
Mating system evolution, resource allocation, and genetic diversity in plants
Plant reproductive ecology
In: Plant Life-History Evolution and Reproductive Ecology (植物生活史进化与繁殖生态学) (ed. Zhang DY (张大勇)), p. 119. Science Press, Beijing. (in Chinese)
An examination of the function of male flowers in an andromonoecious shrub Capparis spinosa
DOI:10.1111/j.1744-7909.2008.00800.x
URL
PMID:19261075
[本文引用: 1]
The pollen donor and pollinator attractor hypotheses are explanations for the functions of the male flowers of andromonoecious plants. We tested these two hypotheses in the andromonoecious shrub Capparis spinosa L. (Capparaceae) and confirmed that pollen production and cumulative volume and sugar concentration of nectar do not differ between male and perfect flowers. However, male flowers produced larger anthers, larger pollen grains and smaller ovaries than perfect flowers. Observations on pollinators indicated that two major pollinators (Xylocopa valga Gerst and Proxylocopa sinensis Wu) did not discriminate between flower morphs and that they transferred pollen grains a similar distance. However, there were more seeds per fruit following hand pollination with pollen from male flowers than from perfect flowers. Individuals of C. spinosa with a larger floral display (i.e. bearing more flowers) received more pollen grains on the stigma of perfect flowers. Female reproductive success probably is not limited by pollen. These results indicate that male flowers of C. spinosa save resources for female function and that they primarily serve to attract pollinators as pollen donors.
