高榕的3类雌花形态及其繁殖特征

榕树(Ficus spp.)及其传粉榕小蜂(Agaonidae)之间经过长期的协同进化, 已形成了高度专一的互惠共生关系。在雌雄同株的榕树中, 同一个榕果内既繁殖种子, 又繁殖榕小蜂, 雌花资源在繁殖种子和榕小蜂之间是怎样分配的?该研究选择广泛分布于西双版纳地区的高榕(F. altissima)及其传粉榕小蜂系统来回答这个问题。高榕果内的雌花柱头形态变异较大, 有3种类型的柱头——球型、弯钩型和火炬型, 它们分别占到雌花总量的54.00%、36.93%和9.07%。3种类型柱头的雌花分别具有不同长度的花柱, 球型柱头雌花的平均花柱长度最短, 火炬型柱头次之, 弯钩型柱头雌花的平均花柱长度最长。在高榕果内, 有传粉者Eupristina altissima和欺骗者Eupristina sp.两类小蜂进入榕果内繁殖, 前者的产卵器长度比96.01%以上的雌花花柱长, 后者的产卵器也要长于85.73%的雌花花柱, 从产卵器长度和雌花花柱长度的匹配情况看, 它们应该可以利用绝大多数雌花产卵繁殖后代。然而, 繁殖榕小蜂的雌花主要是短花柱的雌花, 其中60.64%是球型柱头的雌花; 而繁殖种子的主要是花柱较长的弯钩型柱头和火炬型柱头的雌花。显然, 繁殖榕小蜂和种子的雌花不仅花柱长度有差异, 柱头也分化出了不同的形态, 变异的柱头形状也是调节榕树-榕小蜂繁殖平衡的手段之一。     

聚果榕传粉榕小蜂传粉与产卵之间的权衡

【目的】榕树(Ficus)依赖专性榕小蜂(Agaonidae)传粉,同时为传粉榕小蜂提供繁衍后代的场所,两者形成动植物间经典的协同进化关系。在雌花期果内,榕小蜂需在有限的存活时间内完成传粉和产卵,而传粉榕小蜂如何在传粉与产卵之间进行权衡仍然是悬而未解的问题。本研究旨在明确传粉榕小蜂——一种栉颚榕小蜂Ceratosolen sp.在雌雄同株的聚果榕Ficus racemosa雌花期果内的行为活动及繁殖模式。【方法】借助测微尺测量聚果榕榕果雌花花柱长度与传粉榕小蜂(Ceratosolen sp.)产卵器长度,通过显微视频记录传粉榕小蜂在雌花期果内搜索、传粉及产卵行为;结合单果控制性引蜂试验,测定不同阶段榕小蜂个体大小、孕卵量、携粉量,以及雄花期最终繁殖的榕小蜂后代和榕果种子数量。【结果】聚果榕雌花花柱长度存在树间变异,榕小蜂产卵器长度比绝大多数的雌花花柱长,说明该小蜂可以产卵于大部分的雌花子房里。通常个体大的榕小蜂孕卵量更多,但个体大小与携粉量之间相关性不显著。观察发现,榕小蜂进入雌花期榕果内,前6 h集中产卵,可产下孕卵量的95%,平均搜索用时27 s,产卵用时46 s,此期间传粉行为少见,花粉筐中携带花粉量亦无明显变化;榕小蜂进果后6-24 h,主要执行传粉,其行为主动,连贯高效,单次传粉用时平均为2 s,最终可传完携粉量的80%。控制引蜂试验也证实榕小蜂进入榕果内前6 h主要执行产卵繁殖后代,之后6-24 h主要执行传粉以繁殖榕树种子。【结论】在雌雄同株的聚果榕雌花期榕果内,榕小蜂先产卵、后传粉。本研究首次展示了传粉榕小蜂在聚果榕雌花期榕果内的产卵和传粉行为,并获得与行为相匹配的产卵量和传粉繁殖量,反映了具主动传粉行为的榕小蜂在传粉和产卵之间存在时间和数量上的权衡。     

聚果榕传粉榕小蜂传粉与产卵之间的权衡

【目的】榕树(Ficus)依赖专性榕小蜂(Agaonidae)传粉,同时为传粉榕小蜂提供繁衍后代的场所,两者形成动植物间经典的协同进化关系。在雌花期果内,榕小蜂需在有限的存活时间内完成传粉和产卵,而传粉榕小蜂如何在传粉与产卵之间进行权衡仍然是悬而未解的问题。本研究旨在明确传粉榕小蜂——一种栉颚榕小蜂Ceratosolen sp.在雌雄同株的聚果榕Ficus racemosa雌花期果内的行为活动及繁殖模式。【方法】借助测微尺测量聚果榕榕果雌花花柱长度与传粉榕小蜂(Ceratosolen sp.)产卵器长度,通过显微视频记录传粉榕小蜂在雌花期果内搜索、传粉及产卵行为;结合单果控制性引蜂试验,测定不同阶段榕小蜂个体大小、孕卵量、携粉量,以及雄花期最终繁殖的榕小蜂后代和榕果种子数量。【结果】聚果榕雌花花柱长度存在树间变异,榕小蜂产卵器长度比绝大多数的雌花花柱长,说明该小蜂可以产卵于大部分的雌花子房里。通常个体大的榕小蜂孕卵量更多,但个体大小与携粉量之间相关性不显著。观察发现,榕小蜂进入雌花期榕果内,前6 h集中产卵,可产下孕卵量的95%,平均搜索用时27 s,产卵用时46 s,此期间传粉行为少见,花粉筐中携带花粉量亦无明显变化;榕小蜂进果后6-24 h,主要执行传粉,其行为主动,连贯高效,单次传粉用时平均为2 s,最终可传完携粉量的80%。控制引蜂试验也证实榕小蜂进入榕果内前6 h主要执行产卵繁殖后代,之后6-24 h主要执行传粉以繁殖榕树种子。【结论】在雌雄同株的聚果榕雌花期榕果内,榕小蜂先产卵、后传粉。本研究首次展示了传粉榕小蜂在聚果榕雌花期榕果内的产卵和传粉行为,并获得与行为相匹配的产卵量和传粉繁殖量,反映了具主动传粉行为的榕小蜂在传粉和产卵之间存在时间和数量上的权衡。     

传粉榕小蜂与榕树的繁衍

榕树传粉现象被广泛地作为研究协同进化特别是互惠共生的重要模式之一。本文总结了榕果与传粉榕小蜂的有关研究,试图解释其形态结构之间的相互适应,总结传粉榕小蜂的传粉行为,探讨传粉榕小蜂在雌雄同株及雌雄异株榕树上的传粉模式,讨论传粉榕小蜂的寄主专一性,并展望中国在榕小蜂方面的研究前景。     

榕小蜂温度耐受性及其对种间共存关系的影响

全球已知有约800种榕属(Ficus)植物, 主要分布在热带, 部分种类延伸至亚热带地区。温度是限制榕‒蜂共生系统分布北界的主要因素, 也显著影响榕树及其榕小蜂的繁殖成功, 其中榕小蜂对温度的响应更加敏感。榕小蜂只有在一定的温度范围内才能保持正常的生理机能, 其对温度耐受能力直接影响榕果内小蜂种群数量和群落内种间关系。然而目前对榕小蜂温度耐受性的研究尚少, 榕小蜂的温度耐受能力如何影响榕果内小蜂的共存关系还未见报道。本文研究了分布于西双版纳的2种雌雄同株和1种雌雄异株榕树果内传粉榕小蜂和非传粉小蜂的温度耐受能力。结果表明: 3种传粉榕小蜂对高温的耐受性极差, 相对于雌雄同株的高榕(F. altissima)和聚果榕(F. racemosa)传粉榕小蜂, 雌雄异株的鸡嗉子榕(F. semicordata)传粉榕小蜂对低温有增强的耐受趋势。聚果榕小蜂群落结构显示: 在适宜其生长的西双版纳地区, 传粉榕小蜂的数量占绝对优势, 在温度较低的季节其数量显著减少; 而非传粉榕小蜂呈相反模式, 较强的温度耐受能力使其在低温的雾凉季维持了较高的种群数量。鸡嗉子榕果内非传粉小蜂Sycoscapter trifemmensis相对于Philotrypesis dunia有更强的温度耐受能力, 在种群数量和种间关系上有更多的竞争优势及数量。榕小蜂的温度耐受性差异在物种分布、种间关系的维持和共存上起了重要作用, 本研究结果为阐明榕小蜂种间共存的维持机制提供了科学依据。     

钝叶榕果实内繁殖的两种榕小蜂与寄主榕树间的协同进化

 榕树(Ficus)及其传粉榕小蜂(Agaonidae)构成了高度专一的互惠共生体系。榕树的果实(以下简称榕果)内也寄生着一些非传粉小蜂。 绝大多数非传粉小蜂在榕果外把产卵器刺入果壁产卵到果腔内, 只有极少数种类能够进入果腔内产卵。在西双版纳地区, 钝叶榕(Ficus curtipes)上的杨氏榕树金小蜂(Diaziella yangi)类似于传粉者钝叶榕小蜂(Eupristina sp.), 它也是进入榕果内产卵繁殖后代的, 这就为比 较研究榕果内产卵小蜂与寄主榕树间的关系提供了材料。该文从形态学、行为学和生态学角度比较研究了这两种进入榕果内产卵的小蜂与寄主 钝叶榕之间的作用关系, 研究结果显示: 1)杨氏榕树金小蜂与钝叶榕小蜂的雌蜂头部形状存在趋同进化; 2)两种小蜂的产卵器的平均长度都比 雌花花柱长, 因而能把卵产在子房里; 3)钝叶榕小蜂从瘿花出来需要3~5 h, 交配需要17~19 min, 杨氏榕树金小蜂从瘿花出来只需18~20 min, 交配时间为20~30 s; 4)在自然群落中, 大约90%的雌花期榕果里都只进一只杨氏榕树金小蜂和一只钝叶榕小蜂, 杨氏榕树金小蜂能通过传粉来 增加榕树种子数量, 但对钝叶榕小蜂种群的繁衍造成了极显著的负面影响; 5)两种小蜂于同一时期进入榕果内繁殖, 子代同期成熟羽化, 发育 期与榕树雄花的发育期同步。研究表明: 进入榕果内繁殖的两种小蜂与寄主榕树之间存在着协同进化关系, 杨氏榕树金小蜂为榕树有效地传粉, 这可能是一个由寄生者向互惠方向进化的实例。     

薜荔和爱玉及其传粉昆虫繁殖特性

薜荔(Ficus pumila L．var．pumila)隶属桑科榕属,爱玉(F．pumila L．var．awkeotsanmg Corner)为其变种,它们的花是单性的,雌雄异株。雌花序中着生雌花,雄花序中有瘿花和雄花,每个花序中花的数量极多,达4000～6000朵。薜荔榕小蜂是唯一能进入薜荔和爱玉的隐头花序中产卵或传粉的共生昆虫,自然状态下雌花的结实率分别为82％、83．52％;瘿花的成虫瘿率分别为58．71％、51．32％,因此可形成大量的果实和虫瘿。物候观察表明薜荔和爱玉花期不遇,它们花序中的榕小蜂种群已经生殖隔离。人为的放蜂实验表明,生活于爱玉花序中的榕小蜂,已无法在薜荔花序中繁殖,生殖隔离进一步得到证实;实验同时表明爱玉的花粉亦不能使薜荔雌花结实,宿主两变种间生理上已不亲和。本文从共生双方协同进化的角度出发,探讨了榕树2变种间与传粉昆虫繁殖特性的差异,以及变种产生的主要原因。     

爱玉子花发育的形态学研究

通过花序标记、形态解剖及放蜂实验方法,观察不同发育时期爱玉子雌、雄花序中花的形态特征,以及花发育与小蜂传粉(或产卵)之间的相关性。结果表明,雌前期、雌花期的瘿花在形态上没有明显变化,而雌花的花柱与柱头连成长鞭状,在雌前期呈直立管状,进入雌花期后呈弯曲的S形;在榕小蜂进入花序传粉或产卵5 d后,雌花和瘿花的柱头变黄,花柱开始脱水;在榕小蜂传粉或产卵10 d后,雌花和瘿花花梗伸长,花明显分层,胚迅速发育,子房饱满,花柱和柱头明显萎蔫。传粉小蜂在花序腔内的存活时长不超过3 d。本研究为揭示榕-蜂共生机制提供科学依据。     

天仙果与两种隐头花序小蜂的相互关系

天仙果（Ficus erecta var.beecheyana）花为单性花、雌、雄异株、分别形成雌、雄花序,雌花序着生雌花,雄花序着生雄花和瘿花。花序中生活着银纹榕小蜂（Blastophaga silverstriana）和榕长尾小蜂（Sycoscapter sp.）。前者是唯一能进入雄花序腔产卵或雌花序腔传粉的昆虫,是天仙果专一性共生的传粉者;后者不能进入花序,在花序外通过产卵器将卵产在瘿花子房中,是植食性的寄生者。自然状态下天仙果每个雄花序均被2种小蜂产卵,平均每个花序出飞银纹榕小蜂208.2只、榕长尾小蜂64.2只。人为封堵花序口,银纹榕小蜂无法进入花序产卵,平均每个花序出飞榕长尾小蜂165.6只,是自然状态下的2.5倍,显然,2种小蜂互为竞争对手,榕长尾小蜂是榕-榕小蜂共生体系的破坏者。     

西双版纳热带雨林对叶榕传粉生物学(英)

研究了西双版纳热带雨林地区雌雄异株植物对叶榕 (FicushispidaL .)的生物学、传粉物候学以及榕小蜂(CeratosolensolmsimarchaliMayr)的传粉和繁殖行为。研究结果表明 :雌雄异株的对叶榕与其他雌雄同株的榕属植物不同 ,它的种子形成与传粉者有着更为复杂的相互关系。对叶榕一年结隐花果 6～ 8次 ,结果高峰期 4～ 5次 ,其中雄性植株仅产生花粉和孕育榕小蜂 ,而雌性植株 (无雄蕊 )则需榕小蜂带花粉进入隐花果内 ,进行传粉授精 ,使之发育成种子。对叶榕的成熟花粉不能从花药开裂处自行散发出来 ,必须由榕小蜂采集才能散落。榕小蜂雌蜂羽化、交配后 ,找到雄花区 ,用足、触角、口器在推动中采集花粉。雌蜂飞出熟榕果找寻雌株或雄株榕树上的幼嫩隐花果 ,一般需 3～ 6 7min ;一部分雌蜂在雄株中寻找幼嫩的隐花果 ,进去产卵繁殖 ,另一部分雌蜂则寻找雌株雌花期嫩隐花果进去传粉。雌蜂在雌株榕树的隐花果内传粉时间为 15～ 2 3h ,在雄株榕树的隐花果内产卵时间为 6～ 9h。对叶榕小蜂在雌株上进入单个隐花果的数量多少关系到雌花结实率 ;观察表明 ,每个隐花果最佳进蜂数为 2头 ;榕小蜂传粉后榕树成熟种子形成率在 5 4 .1%～ 82 .5 %之间 ,平均为 73.8% ;而在雄株上雌蜂进蜂数量则关系到榕小蜂在隐花果内的产卵率 ,     

The style–length of the female florets and their fate in two dioecious species of Xishuangbanna, China

Constraints and evolution are central for the resolution of conflicts between mutualism species and for the stability of mutualisms. Dioecious fig species and their specific pollinators are also in conflict on the use of fig ovaries. Here, our experiments provided some data on the female florets allocation in two dioecious fig trees. The results showed that: (1) there is a bimodal distribution in the style–length of two fig trees’ female florets, moreover, the style–lengths are fairly similar and narrowly distributed in gall figs and more variation seems to occur in seed figs; (2) the styles in seed figs are a little longer than those in gall figs; (3) the pollinator's ovipositor lengths are shorter than the style–lengths in seed figs, but they are very similar to those in gall figs so that pollinators can only lay their eggs into the ovaries of gall figs, but not in seed figs; (4) the stigmas stick together, and the style is curly and flexible in seed syconia of the two fig species studied, so it is very difficult for the pollinators to find suitable ovipositing sites and lay their eggs in seed figs; (5) the variations of style-lengths are bigger in seed figs than gall figs, but they are smaller in dioecious figs than monoecious figs; (6) for Ficus cyrtophylla, about 10% styles are shorter in seed figs than those in gall figs, even shorter than ovipositor. In contrast, about 2% styles in gall figs of Ficus hispida are longer than its corresponding pollinator's ovipositor. In a word, our study suggests that the female floret's fate in these two fig species is mainly dependent on its style–length, but not all. The stigma shape and the floral organization can both also attribute to their fate in the two fig species studied.     

Moving your sons to safety: galls containing male fig wasps expand into the centre of figs, away from enemies

Figs are the inflorescences of fig trees (Ficus spp., Moraceae). They are shaped like a hollow ball, lined on their inner surface by numerous tiny female flowers. Pollination is carried out by host-specific fig wasps (Agaonidae). Female pollinators enter the figs through a narrow entrance gate and once inside can walk around on a platform generated by the stigmas of the flowers. They lay their eggs into the ovules, via the stigmas and styles, and also gall the flowers, causing the ovules to expand and their pedicels to elongate. A single pollinator larva develops in each galled ovule. Numerous species of non-pollinating fig wasps (NPFW, belonging to other families of Chalcidoidea) also make use of galled ovules in the figs. Some initiate galls, others make use of pollinator-generated galls, killing pollinator larvae. Most NPFW oviposit from the outside of figs, making peripherally-located pollinator larvae more prone to attack. Style length variation is high among monoecious Ficus spp. and pollinators mainly oviposit into more centrally-located ovules, with shorter styles. Style length variation is lower in male (wasp-producing) figs of dioecious Ficus spp., making ovules equally vulnerable to attack by NPFW at the time that pollinators oviposit. We recorded the spatial distributions of galled ovules in mature male figs of the dioecious Ficus hirta in Southern China. The galls contained pollinators and three NPFW that kill them. Pollinators were concentrated in galls located towards the centre of the figs, NPFW towards the periphery. Due to greater pedicel elongation by male galls, male pollinators became located in more central galls than their females, and so were less likely to be attacked. This helps ensure that sufficient males survive, despite strongly female-biased sex ratios, and may be a consequence of the pollinator females laying mostly male eggs at the start of oviposition sequences.     

Phylogenetic relationships of functionally dioecious FICUS (Moraceae) based on ribosomal DNA sequences and morphology

Figs (Ficus, Moraceae) are either monoecious or gynodioecious depending on the arrangement of unisexual florets within the specialized inflorescence or syconium. The gynodioecious species are functionally dioecious due to the impact of pollinating fig wasps (Hymenoptera: Agaonidae) on the maturation of fig seeds. The evolutionary relationships of functionally dioecious figs (Ficus subg. Ficus) were examined through phylogenetic analyses based on the internal transcribed spacer (ITS) region of nuclear ribosomal DNA and morphology. Forty-six species representing each monoecious subgenus and each section of functionally dioecious subg. Ficus were included in parsimony analyses based on 180 molecular characters and 61 morphological characters that were potentially informative. Separate and combined analyses of molecular and morphological data sets suggested that functionally dioecious figs are not monophyletic and that monoecious subg. Sycomorus is derived within a dioecious clade. The combined analysis indicated one or two origins of functional dioecy in the genus and at least two reversals to monoecy within a functionally dioecious lineage. The exclusion of breeding system and related characters from the analysis also indicated two shifts from monoecy to functional dioecy and two reversals. The associations of pollinating fig wasps were congruent with host fig phylogeny and further supported a revised classification of Ficus.     

Permeability of receptive fig fruits and its effects on the re‐emergence behaviour of pollinators

1. Figs and pollinating fig wasps provide a model system for studying mutualism. The permeability of the syconium changes during receptivity or between seasons, which may affect the behaviour of pollinators. Fig fruits are permeable during receptivity, and in some species, pollinators can enter and re‐emerge after oviposition/pollination. We studied the relationship between fig permeability and pollinator re‐emergence behaviour with a functional dioecious fig, Ficus hispida and the obligate pollinator Ceratosolen solmsi marchali. 2. The relationship reflects the interaction of figs and pollinators in the mutualism and also the conflicts of interests between the two partners: figs benefit from the enclosed fig fruits which have low permeability, but pollinators benefit from their re‐emergence behaviour, which requires high fig permeability. 3. The results showed that at the end of receptivity, the permeability of fig fruits lowered rapidly with changes to the ostiole structures, and re‐emergence rate was low, with more re‐emerging pollinators trapped in the ostiolar bracts. Our results also showed that in the rainy season, the length of receptivity was shorter and fig permeability was lower. The re‐emergence rates were also lower than those in the dry season. The results elucidated that figs' interests dominated in the conflicts between fig and pollinating wasp. 4. Based on a new criteria which employed the classification of pollinators found dead in the ostiolar bracts and which involved a survey of 6 monoecious and 12 dioecious fig species, we found that re‐emergence behaviour was prevalent among fig species, and was more prevalent in functional dioecious figs than monoecious ones.     

Pollination and parasitism in functionally dioecious figs

Fig wasps (Agaonidae: Hymenoptera) are seed predators and their interactions with Ficus species (Moraceae) range from mutualism to parasitism. Recently considerable attention has been paid to conflicts of interest between the mutualists and how they are resolved in monoecious fig species. However, despite the fact that different conflicts can arise, little is known about the factors that influence the persistence of the mutualism in functionally dioecious Ficus. We studied the fig pollinator mutualism in 14 functionally dioecious fig species and one monoecious species from tropical lowland rainforests near Madang, Papua New Guinea. Observations and experiments suggest that (i) pollinating wasps are monophagous and attracted to a particular host species; (ii) pollinating and non-pollinating wasps are equally attracted to gall (male) figs and seed (female) figs in functionally dioecious species; (iii) differing style lengths between gall figs and seed figs may explain why pollinators do not develop in the latter; (iv) negative density dependence may stabilize the interaction between pollinating wasps and their parasitoids; and (v) seed figs may reduce the search efficiency of non-pollinators. This increased pollinator production without a corresponding decrease in seed production could provide an advantage for dioecy in conditions where pollinators are limiting.     

The occurrence of fig wasps in the fruits of female gynodioecious fig trees

Fig trees are pollinated by wasp mutualists, whose larvae consume some of the plant's ovaries. Many fig species (350+) are gynodioecious, whereby pollinators generally develop in the figs of ‘male’ trees and seeds generally in the ‘females.’ Pollinators usually cannot reproduce in ‘female’ figs at all because their ovipositors cannot penetrate the long flower styles to gall the ovaries. Many non-pollinating fig wasp (NPFW) species also only reproduce in figs. These wasps can be either phytophagous gallers or parasites of other wasps. The lack of pollinators in female figs may thus constrain or benefit different NPFWs through host absence or relaxed competition. To determine the rates of wasp occurrence and abundance we surveyed 11 dioecious fig species on Hainan Island, China, and performed subsequent experiments with Ficus tinctoria subsp. gibbosa to identify the trophic relationships between NPFWs that enable development in female syconia. We found NPFWs naturally occurring in the females of Ficus auriculata, Ficus hainanensis and F. tinctoria subsp. gibbosa. Because pollinators occurred only in male syconia, when NPFWs also occurred in female syconia, overall there were more wasps in male than in female figs. Species occurrence concurred with experimental data, which showed that at least one phytophagous galler NPFW is essential to enable multiple wasp species to coexist within a female fig. Individuals of galler NPFW species present in both male and female figs of the same fig species were more abundant in females than in males, consistent with relaxed competition due to the absence of pollinator. However, these wasps replaced pollinators on a fewer than one-to-one basis, inferring that other unknown mechanisms prevent the widespread exploitation by wasps of female figs. Because some NPFW species may use the holes chewed by pollinator males to escape from their natal fig, we suggest that dispersal factors could be involved.     

Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): hypotheses for an ancient symbiosis

Figs and their pollinating fig wasps are dependent on one another for propagation of their own kinds. The wasps reproduce by ovipositing through the styles of female flowers within the closed fig receptacles (syconia). About half of the female flowers within the syconia of monoecious figs have styles which are longer than the ovipositors of the wasp, and they will therefore produce seeds rather than wasp larvae. Since a longer ovipositor would enable a wasp to reach more ovules and deposit more eggs, the question arises at to why longer ovipositors have not evolved.
In an attempt to answer this question, four seemingly plausible hypotheses are examined but each is shown to be problematical in some way. Consideration is then given to a fifth hypothesis which proposes that ovipositor length is constrained by abortion of syconia with relatively few seed embryos and many agaonid larvae. It is argued first that this pattern of abortion will be selected during a sustained period of heavy wasp infestation because seeds will then become scarce relative to pollen-carrying wasps. Increased expenditure by the fig on seed production would therefore be favoured by natural selection. A greater expenditure on seeds would occur if young syconia with exceptionally heavy wasp infestations were dropped and the saved nutrients invested in syconia of a subsequent crop containing average levels of wasp larvae and seeds. Provided that the energy and nutrient cost of dropping young syconia is small, the selective advantage to the wasp of longer ovipositors is eliminated in this way. A stable coexistence of figs and wasps is therefore possible. The paper concludes by discussing two general predictions of the abortion hypothesis, and how these may be tested.     

Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology

The obligate mutualism between pollinating fig wasps in the family Agaonidae (Hymenoptera: Chalcidoidea) and Ficus species (Moraceae) is often regarded as an example of co-evolution but little is known about the history of the interaction, and understanding the origin of functionally dioecious fig pollination has been especially difficult. The phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus were inferred from mitochondrial cytochrome oxidase gene sequences (mtDNA) and morphology. Separate and combined analyses indicated that the pollinators of functionally dioecious figs are not monophyletic. However, pollinator relationships were generally congruent with host phylogeny and support a revised classification of Ficus. Ancestral changes in pollinator ovipositor length also correlated with changes in fig breeding systems. In particular, the relative elongation of the ovipositor was associated with the repeated loss of functionally dioecious pollination. The concerted evolution of interacting morphologies may bias estimates of phylogeny based on female head characters, but homoplasy is not so strong in other morphological traits. The lesser phylogenetic utility of morphology than of mtDNA is not due to rampant convergence in morphology but rather to the greater number of potentially informative characters in DNA sequence data; patterns of nucleotide substitution also limit the utility of mtDNA findings. Nonetheless, inferring the ancestral associations of fig pollinators from the best-supported phylogeny provided strong evidence of host conservatism in this highly specialized mutualism.     

Differentiation during fig ontogeny suggests opposing selection by mutualists

Dioecy allows separation of female and male functions and therefore facilitates separate co‐evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower‐stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male (“gall”) figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female (“seed”) figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.