两种Eupristina属小蜂对宿主榕果挥发物和合成信息素的行为反应

高榕,雌雄同株,与其共生的形态高度相似的传粉小蜂Eupristina altissima与非传粉小蜂Eupristina sp.均为果内产卵。利用Y型嗅觉仪生物测定法研究E.altissima和Eupristina sp.对不同发育期高榕榕果挥发物以及合成信息素混合物的行为反应差异。结果表明:E.altissima和Eupristina sp.对高榕雌花期榕果挥发物具极显著趋向行为,对高榕雄花期榕果挥发物具极显著驱避行为,表明E.altissima与Eupristina sp.雌蜂能够敏锐辨别高榕雌花期和雄花期榕果的挥发物,快速远离雄花期榕果,并实现对宿主雌花期榕果的定位。但是,E.altissima与Eupristina sp.对其它发育时期榕果挥发物的行为反应具有差异性,前者对雌前期榕果和传粉或产卵后榕果释放的挥发物存在显著的趋避反应,而后者无明显的行为偏向性,表明E.altissima能够识别雌前期榕果和传粉或产卵后榕果,可避免误入其中而无法繁殖后代,Eupristina sp.则不具备这种识别能力。E.altissima和Eupristina sp.小蜂对合成信息素的行为反应也高度相似,表现为芳樟醇、苯乙烯,以及苯乙烯和金合欢醇的交互作用对两种小蜂选择行为影响显著,组合A_1B_2C_2(0.5%Linalool+1%Benzyl ethylene+1%Farnesol)的混合信息素对两种小蜂具有极显著的驱避作用,而组合A_2B_1C_1(1%Linalool+0.5%Benzyl ethylene+0.5%Farnesol),A_2B_1C_2(1%Linalool+0.5%Benzyl ethylene+1%Farnesol),A2B2C1(1%Linalool+1%Benzyl ethylene+0.5%Farnesol)的混合信息素对其具有极显著的吸引作用,但两种小蜂对组合A_1B_1C_1(0.5%Linalool+0.5%Benzyl ethylene+0.5%Farnesol)的行为反应存在差异。两种小蜂对榕果挥发物和合成信息素的反应异同,可能与其触角结构的差异密切相关。研究结果为探究榕-蜂共生体系的化学信号传导机制提供科学依据。     

信息化合物对薜荔榕小蜂选择行为的影响

爱玉子和薜荔均为桑科榕属植物,与薜荔榕小蜂保持稳定的共生关系,信息化合物在维系榕树与其传粉小蜂的共生关系中起决定性作用。应用Y型嗅觉仪检测两种来源的薜荔榕小蜂对8种单一信息化合物和芳樟醇、苯甲醇和松油醇组成的混合信息化合物的趋向性反应。实验结果表明:3%和5%芳樟醇、5%的苯乙烯、7%苯甲醇、5%和7%松油醇以及7%金合欢醇对两种来源的薜荔榕小蜂均具有显著的吸引作用,7%苯甲酸甲酯对两种来源的薜荔榕小蜂有显著的趋避作用,香兰醛对两种来源的薜荔榕小蜂的行为没有显著的影响,从而表明信息化合物的种类和浓度均显著影响薜荔榕小蜂的选择行为。5%芳樟醇、3%松油醇和3%苯甲醇的混合信息化合物组合对两种来源的薜荔榕小蜂具极显著的吸引作用,信息化合物之间的交互作用极为显著。两种不同来源的薜荔榕小蜂对信息化合物反应的异同,表明两种不同来源的薜荔榕小蜂与各自宿主之间的化学通讯信号传导上存在差异,同时也表明两种不同来源的薜荔榕小蜂之间存在密切的亲缘关系。在榕树接受期花序的挥发物成分中广泛存在并占较大比例的信息化合物(例如芳樟醇),可能与榕小蜂对寄主的远程定位有关,而近距离的专性定位却是依赖于各种信息化合物严格按一定浓度、比例组成的化学图谱。实验结果为榕-蜂共生体系的化学生态学理论研究和爱玉子高产栽培提供科学依据。     

传粉榕小蜂与非传粉小蜂间寄主识别行为的趋同进化

在高度专性传粉的榕树-榕小蜂互惠共生系统中普遍存在着一些非传粉小蜂,它们中的一些种类进入果腔后也能为榕树传粉,且在形态和物候上已与传粉榕小蜂发生了趋同进化。但其寄主识别行为是否也与传粉榕小蜂发生了趋同进化还不得而知。我们在西双版纳选择了钝叶榕(Ficuscurtipes)及其3种进果繁殖小蜂开展了相关的行为实验。3种小蜂中,1种是钝叶榕的专性传粉榕小蜂(Eupristina sp.),另外2种是寄居性非传粉小蜂(杨氏金小蜂Diaziellayangi和Lipothymus sp.),这2种非传粉小蜂进入果腔后也像传粉榕小蜂那样为钝叶榕传粉。我们以钝叶榕不同发育时期的榕果及这3种小蜂为材料,采用Y型嗅觉仪观察了这3种小蜂对各发育时期榕果和信息化学物质6-甲基-5-庚烯-2-醇、6-甲基-5-庚烯-2-酮及这2种化合物的混合物的选择行为。结果表明,当提供雌花期榕果与其他发育时期榕果和空气对照供这3种小蜂选择时,它们均显著地偏向于选择雌花期榕果;当提供雄花期榕果与其他发育时期榕果和空气对照供这3种小蜂选择时,它们均显著地偏向于选择其他发育时期榕果和空气对照,即都会避开雄花期榕果;此外,这3种小蜂均对钝叶榕雌花期果释放的一种主要化合物6-甲基-5-庚烯-2-醇的同一剂量(1μL)表现出显著的偏好。这一结果为传粉榕小蜂与非传粉小蜂间的寄主识别行为趋同进化的假说提供了证据。     

爱玉子花序挥发物成分以及对其传粉小蜂的吸引作用

利用动态顶空吸附法和GC-MS分析,研究接受期以及传粉或产卵5d后爱玉子(Ficus awkeotsang)雌、雄隐头花序挥发物成分。研究结果表明:爱玉子隐头花序挥发物的组成成分复杂,种类繁多,主要成分是对传粉小蜂具有显著吸引作用的芳樟醇。组成雌、雄花序的接受期挥发物信号的化合物种类与数量不同,但两者之间的共有化合物却占花序挥发物总量的70%以上,且接受期雌、雄花序挥发物组成比例相似,小蜂无法通过花序挥发物信号的差异,区别雌、雄花序,从而支持"榕树雌、雄花序接受期挥发物存在相互模拟现象"的假说。爱玉子传粉(或产卵)前后花序挥发物信号发生变化,表现在花序在传粉(或产卵)后,一些挥发性化合物在榕果中消失或相对含量减少(如芳樟醇),有些化合物的相对含量增加(如苯甲酸甲酯),并出现新的化合物(如2-乙基己醇);在化合物组成上,萜类化合物相对含量下降,芳香族化合物、脂肪族化合物相对含量上升。嗅觉仪实验表明爱玉子接受期雌、雄花序挥发物对其传粉榕小蜂有极显著的吸引作用,而传粉(或产卵)5d后的雌、雄花序挥发物对传粉榕小蜂有显著的趋避作用。传粉小蜂对雌、雄接受期花序挥发物的选择没有偏向性。榕果通过挥发物的释放量和成分的改变反映出花发育与被授粉(被产卵)状况,传粉小蜂通过接收榕果发出的化学信息,判断选择适合的寄主。研究对于爱玉子的高产栽培以及植物与昆虫专性共生化学生态学机制的理论研究具有重要的意义。     

榕树隐头花序挥发物组成及其传粉榕小蜂寄主识别行为

榕树(Ficus spp.)通过挥发性化学物质来吸引传粉榕小蜂(Agaonidae),这种特异性的化学信号释放存在着两种模式,一种是释放多种化合物的"泛化"模式,另一种是释放不常见单一化合物的"专化"模式。为揭示榕树(Ficus microcarpa)及其传粉榕小蜂Eupristina verticillata之间的化学通讯机制,该研究采用固相微萃取法提取榕树隐头花序不同发育期(花前期、雌花期传粉前后、间花期、雄花期和花后期)释放的挥发物,并用气相色谱-质谱联用仪鉴定挥发物成分,分析其变化动态,再通过Y型嗅觉仪检测榕树传粉榕小蜂对各发育期隐头花序的行为反应。结果表明:榕树隐头花序释放的挥发性化合物共鉴定出21种,主要是脂肪酸衍生物、萜类化合物和芳香族化合物。不同发育期隐头花序的挥发物组分差异明显,雌花期传粉前后的挥发物差异表现为传粉后萜类化合物含量下降,脂肪酸衍生物含量增加,特别是传粉前含量较高的特征化合物2-庚酮和3-辛酮消失,D-柠檬烯含量下降,而可巴烯、环己烷和2-己烯醛含量上升。行为检测的结果也表明:雌花期隐头花序对传粉榕小蜂的吸引作用最强,而雄花期的隐头花序释放的挥发物对传粉榕小蜂有趋避作用,形成了对传粉榕小蜂"推拉"的互作模式。有多种化合物在榕树传粉榕小蜂的寄主识别过程中发挥作用,表明榕树及其传粉榕小蜂的互惠共生关系是通过多种化合物的"泛化"策略来维系的。     

榕果挥发物对传粉榕小蜂的吸引作用

榕树 /榕小蜂专一性共生系统的维持 ,与榕树开花期释放的特殊的挥发性化合物以及榕小蜂对其寄主榕树的化学识别和定位紧密相关。研究选取了西双版纳地区常见的 3种榕树 ,即对叶榕 Ficus hispida、木瓜榕 F.auriculata和鸡嗉子榕F.semicordata的榕果作为实验材料 ,利用野外诱捕实验、室内生物检测实验检测传粉榕小蜂 Hymenoptera:ChalcidoidaeAgaonidae对 12种信息化合物及榕果的二氯甲烷浸提物的趋向性反应 ,研究不同榕属植物的传粉榕小蜂对相同的信息化合物的反应差异 ,以及传粉榕小蜂受不同发育时期榕果浸提物吸引的显著性程度。诱捕实验中对叶榕小蜂 Ceratosolen solmsimarchali对香叶醇的趋向性反应显著 ,大果榕小蜂 C.emarginatus对接受期榕果浸提物和芳樟醇都有明显的趋向性反应 ,而对间花期榕果浸提物则无显著反应。嗅觉仪生物检测实验中 ,鸡嗉果榕小蜂 C.gravelyi对香叶醇和松油醇都表现出显著的趋向性反应。结果表明 ,对叶榕、鸡嗉子榕传粉榕小蜂对 12种信息化合物的反应存在一定的差异 ,木瓜榕传粉榕小蜂对香叶醇和木瓜榕接受期榕果浸提物的趋向性反应比间花期榕果强得多     

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。     

对叶榕花序不同发育时期气味成分的变化及其对传粉者的吸引作用

为探讨榕果发育过程中气味挥发物的动态变化及其对传粉者行为的调节作用,比较对叶榕(Ficus hispia)不同发育时期花序挥发物的变化,并结合Y形嗅觉仪检测对叶榕传粉榕小蜂对不同花序的选择性。结果表明,在3个发育时期的花序中共检测到64种化合物,对叶榕采用"泛化"策略吸引传粉榕小蜂,十一烷、β-榄香烯、β-芹子烯、α-依兰油烯可能是对传粉榕小蜂起吸引作用的物质。雌前期花序气味与雌花期相似,间花期与雌前期、雌花期的有显著差异,传粉榕小蜂对雌前期和雌花期花序具有明显的选择倾向,对间花期花序表现出驱避性,表明对叶榕与传粉者存在"推-拉"作用模式。雌前期花序释放的气味,有助于传粉者对寄主的定位。同一时期个体间的气味成分存在空间异质性,这种异质性在间花期更加显著,表明气味成分受环境影响。间花期花序气味由于不需要特异性地吸引传粉者,因而更容易发生变化。这有助于更好地理解榕树挥发性物质的组成特点,以及化学机制在维持榕树-榕小蜂共生体系中的关键作用。     

基于28S, COI和Cytb基因序列的薜荔和爱玉子传粉小蜂分子遗传关系研究

薜荔和爱玉子均属于桑科榕属植物,二者为同一物种的原变种与变种的关系,早期研究认为这两种榕树与同一种传粉榕小蜂(Wiebesia pumilae (Hill))建立了稳定的互利共生关系,但近期在形态学、生态学、传粉生物学等方面对二者的研究结果表明,薜荔传粉小蜂和爱玉子传粉小蜂之间可能发生了遗传分化。实验用核糖体28SrDNAD1-D3区、线粒体Cytb及COI基因部分序列,对采自福建3个不同样地的薜荔传粉小蜂和3个不同品系的栽培爱玉子的传粉小蜂进行分析,结果表明:(1)薜荔传粉小蜂和爱玉子传粉小蜂的核糖体28S序列的碱基组成中A,T,G,C 4种含量较平均,C+G的平均含量(56%)稍高于A+T的含量(44%)。线粒体Cytb序列中A+T的含量(76.1%)明显高于C+G的含量(23.9%),COI序列中A+T的含量(71.9%)也明显高于G+C的含量(28.1%),这是膜翅目昆虫线粒体基因的普遍特征。在薜荔和爱玉子传粉小蜂的线粒体Cytb及COI基因中,密码子第三位点A+T的含量最高。(2)比较薜荔和爱玉子传粉小蜂的3种分子标记的变异范围显示,28S进化速度较Cytb及COI序列慢,比较保守,更适合科、亚科等较高分类单元的研究。薜荔传粉小蜂与爱玉子传粉小蜂之间的亲缘关系较近,采用Cytb与COI序列进行分析更为精确。(3)用Cytb及COI序列对薜荔传粉小蜂与爱玉子传粉小蜂之间的遗传距离进行分析显示,薜荔传粉榕小蜂个体间Cytb序列平均遗传距离为0.0054,爱玉子传粉小蜂个体间的Cytb遗传距离为0.0164;薜荔传粉小蜂与爱玉子传粉小蜂群体之间的Cytb序列平均遗传距离为0.1385;COI序列的薜荔传粉榕小蜂个体间遗传距离为0.0048,爱玉子传粉小蜂各样本间平均遗传距离为0.0102;薜荔传粉小蜂与爱玉子传粉小蜂群体间COI序列平均遗传距离为0.1896,两群体间的遗传距离(差异大于10%以上)明显大于群体内各样本之间的遗传距离,表明薜荔传粉小蜂与爱玉子传粉小蜂之间已经发生了很大的遗传分化,其变异水平达到了种间分化水平,即薜荔传粉小蜂与爱玉子传粉小蜂为两个不同的种。     

高榕雌花期传粉榕小蜂和欺骗性小蜂的繁殖特点

榕树及其专一性传粉榕小蜂组成了动植物界最为经典的协同进化关系,传粉榕小蜂演化出欺骗性是非常罕见的。在雌雄同株的高榕隐头果内,共存着一种传粉榕小蜂Eupristina altissima和一种欺骗性的小蜂Eupristina sp.,两种小蜂在雌花期进入隐头果内繁殖,但有不同的繁殖特点。对比研究了两种小蜂从成虫羽化到产卵和传粉这个阶段的雌蜂个体大小、孕卵量及繁殖差异,结果表明:羽化期两种雌蜂的平均个体小,经飞行小个体的雌蜂易死亡,大个体雌蜂到达接受树,但通过苞片通道,一些个体较大的传粉榕小蜂被夹死导致进入果腔的雌蜂相对小,而欺骗性小蜂易通过苞片以至进入果腔的雌蜂个体较大。两种未产卵雌蜂均表现为个体大者孕卵量较多,但两种雌蜂的平均孕卵量没有差异。即使有充足雌花资源产卵,两种雌蜂均未产完所有卵,产卵后两种雌蜂卵巢中的卵量均显著减少,遗留下的卵量两种小蜂间没有差异。传粉榕小蜂只有部分个体传完所携带花粉,并表现为传粉越成功的雌蜂,产卵越多。存在种内竞争时,两种小蜂的产卵量均减少,传粉榕小蜂的传粉效率也降低。在种间竞争背景下,欺骗性小蜂产卵更成功,传粉榕小蜂的产卵和传粉量均受到极大抑制。研究结果说明雌花期隐头果内传粉榕小蜂只适量利用雌花资源产卵繁殖后代,更有效地传粉繁殖榕树种子,这可能是维持榕-蜂互惠系统稳定共存的重要机制之一;欺骗者稳定存在需降低与传粉者的直接竞争,而欺骗者和传粉者分散在不同果内,甚至是不同的树上繁殖是理想的繁殖策略。     

鸡嗉子榕隐头果雌花期特征对传粉榕小蜂选择的影响

为了探讨榕树隐头果的发育期、性别、大小等外部特征对传粉榕小蜂选择的影响,采取人为控制雌花期的方法,对鸡嗉子榕(Ficus sermicordata)及其传粉榕小蜂(Ceratosolen gravelyi)的选择行为进行研究。结果表明,在隐头花序发育到雌花期后,如果阻止传粉小蜂进入,隐头果会继续生长。直径较小的雌果和雄果的进蜂量较多,且在雌雄果同时存在时,小蜂仍然会选择进入雌果,但进蜂量显著低于雄果。小蜂优先选择进入雌花期前期的隐头花序,雌雄果皆有此特点。对于相同发育期的隐头果,果径和进蜂量呈正相关关系,说明对于相同发育期的隐头果,小蜂更倾向于进入较大的隐头果。因此,真正控制小蜂行为的是隐头花序所处的发育期,以及不同发育期所产生的化学挥发物,而非隐头果直径大小。这为进一步研究榕-蜂系统的稳定机制提供依据。     

Different Stimuli Reduce Attraction to Pollinators in Male and Female Figs in the Dioecious Fig Ficus hispida

Fig trees ( Ficus ) and their obligate pollinating wasps (Hymenoptera, Chalcidoidea, Agaonidae) are a classic example of a coevolved mutualism. Pollinating wasps are attracted to figs only when figs are receptive. It has been shown that figs will lose their attraction to pollinators sooner in monoecious and male dioecious figs when multiple pollinators have entered the enclosed inflorescence. However, little is known about the nature of the stimulus inducing the loss of attraction. By conducting experiments on the functionally dioecious fig, Ficus hispida , we show that (1) different stimuli induce the loss of attraction in each sex, pollination in female figs, and oviposition in male figs; and (2) foundress number affects the loss of attraction in both sexes only when the prerequisites ( i.e ., pollination in female figs and oviposition in male figs) have been satisfied. In general, the more foundresses that enter, the earlier the fig will lose its receptivity. We argue that the stimuli in male and female figs are adaptations to the fulfillment of its respective reproduction.     

榕树高度专性共生体系内影响传粉蜂子代繁殖的因素

为探讨影响传粉蜂子代数量及性比的因素,以广州地区分布的粗叶榕(Ficus hirta Vahl)及其传粉小蜂爪哇榕小蜂(Valasia javana Mayr)为材料,采用自然收蜂与控制放蜂试验进行研究。结果表明,果内的榕小蜂群落随季节更替发生显著变化,非传粉蜂的介入、季节差异使雌蜂间的干扰强度不同,导致传粉蜂子代数量发生变化,其中雌蜂间的干扰会使传粉蜂性比显著升高,而非传粉蜂的介入对传粉蜂性比的影响不大,传粉蜂仍能正常地进行繁殖。另外,传粉蜂在雌花期雄花序内的产卵和存活时间一般较短,约为15 h;传粉蜂子代在干、湿季的雄花序内的发育时间差异显著,干季时间长,湿季时间短。这表明传粉榕小蜂进化出了适应广州地区季节变化的繁殖策略。     

The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.     

Between‐species facilitation by male fig wasps in shared figs

1. Facilitation is recorded from diverse plant–insect interactions, including pollination and herbivory. 2. The significance of facilitation resulting from the behavior of males of multiple fig wasp species inside figs was investigated. Female fig wasps emerge from natal figs via exit holes dug by males, especially male pollinators. When no males are present, the females struggle to escape and may die. 3. Ficus microcarpa L. is a widely‐established invasive fig tree from Southeast Asia. Its pollinator is absent in South Africa, so the tree cannot reproduce, but two Asian non‐pollinating fig wasps (NPFW) Walkerella microcarpae and Odontofroggatia galili occupy its figs. Abundance patterns of the two NPFW and the proportion of male‐free figs in South Africa, Spain (where the pollinator is introduced), and in China, where the native fig wasp community is diverse, were compared to determine the consequences of reduced species richness for insect survival. 4. Female fig wasps in male‐free figs were found to be trapped, and small clutch sizes contributed to the absence of males in both species. The presence of pollinators in Spain allowed most NPFW to develop in figs containing males. Far more male‐free figs were present in South Africa, elevating mortality rates among female NPFW. Facilitation of female release by males of other NPFW species nonetheless benefitted the rarer species. 5. Selection pressures in South Africa currently favour greater aggregation of NPFW offspring and/or less female biased sex ratios.     

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

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.     

POLLINATOR‐MEDIATED REPRODUCTIVE ISOLATION AMONG DIOECIOUS FIG SPECIES (FICUS,MORACEAE)

The extent of isolation among closely related sympatric plant species engaged in obligate pollination mutualisms depends on the fitness consequences of interspecies floral visitation. In figs (Ficus), interspecific gene flow may occur when pollinating wasps (Agaonidae) visit species other than their natal fig species. We studied reproductive isolation in a clade of six sympatric dioecious fig species in New Guinea. Microsatellite genotyping and Bayesian clustering analysis of the fig community indicated strong reproductive barriers among sympatric species. A total of 1–2% of fig populations consisted of hybrid individuals. A new experimental method of manipulating fig wasps investigated the reproductive consequences of conspecific and heterospecific pollinator visitation for both mutualists. Fig wasps introduced to Ficus hispidioides pollinated and oviposited in receptive figs. Seed development and seedling growth were largely comparable between conspecific and heterospecific crosses. Heterospecific pollinator fitness, however, was significantly less than that of conspecific pollinators. Heterospecific pollinators induced gall formation but offspring did not develop to maturity in the new host. Selection on pollinators maintaining host specificity appears to be an important mechanism of contemporary reproductive isolation among these taxa that could potentially influence their diversification.