生态学报  2015, Vol. 35 Issue (12): 3988-3999

文章信息

王小艺, 杨忠岐, 魏可, 唐艳龙
WANG Xiaoyi, YANG Zhongqi, WEI Ke, TANG Yanlong
昆虫翅型分化的表型可塑性机制
Mechanisms of phenotypic plasticity for wing morph differentiation in insects
生态学报, 2015, 35(12): 3988-3999
Acta Ecologica Sinica, 2015, 35(12): 3988-3999
http://dx.doi.org/10.5846/stxb201310302610

文章历史

收稿日期:2013-10-30
修订日期:2014-08-28
昆虫翅型分化的表型可塑性机制
王小艺, 杨忠岐 , 魏可, 唐艳龙    
中国林业科学研究院森林生态环境与保护研究所, 国家林业局森林保护学重点实验室, 北京 100091
摘要:翅多型现象在昆虫中广泛存在,是昆虫在飞行扩散和繁殖能力之间权衡的一种策略,对种群的环境适应性进化具有重要的意义。目前在植食性昆虫中研究较多,有关寄生蜂的翅型分化鲜见报道。综述了昆虫翅型分化的表型可塑性机制。遗传因素和环境因素均对昆虫翅的发育产生影响,基因型对翅型的决定具有显著作用,外界环境条件,包括温度、光周期、食物质量、自身密度、外源激素等因素对昆虫翅的发育也产生重要的调节作用,从而产生翅的非遗传多型性现象。此外,天敌的寄生或捕食作用可能会诱导某些昆虫的翅型产生隔代表型变化。对昆虫产生翅多型现象的生态学意义及其在生物进化过程中的作用进行了讨论,并探讨了寄生性昆虫翅型分化机制在生物防治上的可能应用途径。功能基因组学和表观遗传学的进一步发展可望为彻底揭示昆虫翅型分化机制提供新的机遇和技术手段。
关键词翅多型性    非遗传多型性    表型可塑性    适应性进化    
Mechanisms of phenotypic plasticity for wing morph differentiation in insects
WANG Xiaoyi, YANG Zhongqi , WEI Ke, TANG Yanlong    
Key Laboratory of Forest Protection, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
Abstract:Phenotypic plasticity is a phenomenon in which the same genotype produces entirely different phenotypes in response to changes in the environment, and grants an organism the ability to adapt to environmental variations. Wing polymorphism is commonly observed in insects, including Homoptera, Hemiptera, Coleoptera, Hymenoptera, Orthoptera, Diptera, Lepidoptera, Isoptera, Psocoptera, and Dermaptera, as a strategy to tolerate trade-offs between flight capability and fecundity. As a result, it may confer an important adaptive value to the evolution of populations because these winged individuals can migrate long distances and find suitable habitats for development and reproduction of their offspring more easily. At the present time, there is limited knowledge of the mechanisms of wing polymorphism in varying populations. Both genes and the environment are usually considered to affect the developmental outcomes of insect wing morphs. It is easy to understand the contributions of genes to morphology as a consequence of the research of evolution and developmental biology. However, very little is known about the influential mechanism of environmental factors on the development of phenotypes. In fact, it is not yet clear that how the evolutionary shifts of character variation is realized between environmental and genetic control. So far, studies on wing polymorphism are mostly reported on phytophagous insects, very few are known in parasitoids, natural enemies of insect pests. Here we summarized the mechanisms of phenotypic plasticity for wing morph differentiation in insects. Both genetic and environmental factors can act on the wing development of insects. The genotypes have significant effects on the determination of insect wing morphs. External environmental conditions such as temperature, photoperiod, food quality, population density, exogenous hormones, etc., also play important roles in regulating the insect wing development, which produce wing polyphenism. In addition, the parasitism or predation of natural enemies may induce alternative variations across transgenerational wing morphs in some insects. The ecological significance of insect wing polymorphism and its functions during their evolutionary process are discussed. Polyphenism is one of the main reasons why insects have become so successful on the earth, and grants them the capability to effectively utilize the same genome in order to best adapt to predictable changes in the environment, such as degradation of survival conditions after overcrowding, by developing into different phenotypes. Wing polyphenism in insects is a clear example of adaptive phenotypic plasticity, which provides a very good model to study alternative phenotypes from both genetic and environmental perspectives. This may also be advantageous to evaluate how environmental and genetic factors jointly control the same developmental events. Further study recommendations were also discussed in this review, as well as the potential utilization of wing morph differentiation mechanisms of parasitic wasps in biological control, e.g., through artificially culturing the winged individuals of parasitoids for field release to improve the dispersal ability of natural enemies. Some critical aspects still need to be investigated further on the mechanisms of phenotypic plasticity for wing morph differentiation in insects. Further development in functional genomics and epigenetics may provide novel opportunities and technological support for revealing the mechanisms of polyphenism in insects completely.
Key words: wing polymorphism    polyphenism    phenotypic plasticity    adaptive evolution    

表型可塑性是指同一基因型因受不同的环境影响而产生不同表现型的现象[1],是生物对环境变化的一种适应。昆虫的翅多型现象在同翅目、半翅目、鞘翅目、膜翅目、直翅目、双翅目、鳞翅目、等翅目、啮虫目以及革翅目中广泛存在(表 1),这对种群的适应性具有十分重要的意义。因为具翅型可以远距离扩散、找到更合适的栖境供后代生存和繁衍。翅二型性昆虫是研究扩散进化的优良材料,翅的二型性是昆虫在飞行能力和繁殖能力之间权衡的一种策略,但种群保持翅型分化的机制目前仍不清楚。通常认为遗传基因和环境因素均对昆虫翅型的决定产生影响[2, 3, 4]。本文总结了昆虫翅型分化的表型可塑性机制,以期指导寄生性天敌昆虫在生物防治上的有效利用。

表 1 具有翅型分化特性的昆虫类别及影响翅生长发育的主要因素 Table 1 Insects with wing dimorphism and major impact factors of wing development

Order

Family
种类
Species
有翅或长翅
Winged or Macropterous
食性
Feeding habits
参考文献
Reference
本表不包括因性二型性所产生的翅型差异
同翅目
Homoptera
蚜科Aphididaec 豌豆蚜Acyrthosiphon pisum 高密度、天敌 植食性 [25, 36, 45, 46, 47, 48]
棉蚜Aphis gossypii 高密度、寄主病毒 植食性 [27, 49]
红秋麒麟蚜
Uroleucon nigrotuberculatum
天敌 植食性 [50]
麦二叉蚜Schizaphis graminum 高密度 植食性 [40]
麦长管蚜Sitobion avenae 高密度、食物短缺 植食性 [25]
桃蚜Myzus persicae 低温、高密度、食物短缺、杀虫剂 植食性 [51, 52, 53]
飞虱科Delphacidae 白背飞虱Sogatella furcifera 高密度、长日 照、营养不足 植食性 [32]
褐飞虱Nilaparvata lugens 保幼激素水平低、高密度、 高温和短日照 植食性 [54, 55, 56, 57]
直翅目
Orthopteran
蝼蛄科Gryllotalpidae 东方蝼蛄Gryllotalpa orientalis 营养不足 植食性 [10]
螽斯科Tettigoniidae 美国山魁姬螽Metrioptera roeselii 高密度 植食性 [58]
锥头蝗科
Pyrgomorphidae
臭腹腺蝗Zonocerus variegatus 旱季 植食性 [59]
蟋蟀科Gryllidae 东南田蟋Gryllus rubens 单独饲养(低密度)、保幼激素水平低、短日照 植食性 [60, 61, 62]
沙蟋Gryllus firmus 保幼激素水平低、脂类吸收增加 植食性 [63, 64]
热带家蟋Gryllodes supplicans 高密度且同时高温 植食性 [65]
黑胫草蟋蟀
Trigonidium cicindeloides
高密度 植食性 [65]
南方地蟋Allonemobius socius 高密度、高温、长日照及其交互作用 植食性 [43]
迷卡斗蟋Velarifictorus micado 高密度 植食性 [66]
长颚斗蟋V. asperses 高密度、高温和长光照 植食性 [67]
曲脉姬蟋
Modicogryllus confirmatus
保幼激素水平低 植食性 [68]
鞘翅目
Coleoptera
象甲科Curculionidae 苜宿叶象甲Hypera postica 高密度、高温 植食性 [26]
豆象科Bruchidae 四纹豆象
Callosobruchus maculatus
高密度、高温、短日照和水分低的食物 植食性 [69]
步甲科Carabidae 黑通缘步甲
Pterostichus melanarius
不稳定的栖境条件 捕食性 [70]
半翅目
Hemiptera
长蝽科 Lygaeidae 甘蔗长蝽Cavelerius saccharivorus 高密度、长日照、高温 植食性 [71]
高粱长蝽
Dimorphopterus japonicus
高密度、长日照、高温 植食性 [44, 72]
麦小长蝽Nysius huttoni 长光周期和高温 植食性 [41]
南部长蝽Blissus insularis 高密度 植食性 [73]
红蝽科Pyrrhocoridae 先地红蝽Pyrrhocoris sibiricus 高温和短日照 植食性 [74]
始红蝽P. apterus 高温和长日照 植食性 [74]
黾蝽科Gerridae 水黾Aquarius najas 短日照、高温 捕食性 [75]
道氏广肩水黾Microvelia douglasi 高密度、高温、长日照和 食物短缺 捕食性 [42]
革翅目
Dermaptera
蠼螋科Labiduridae 热带蠼螋Paralabella dorsalis 食物短缺 捕食性 [76]
鳞翅目
Lepidoptera
毒蛾科Lymantriidae 白点毒蛾Orgyia thyellina 长日照、高温 植食性 [77]
双翅目
Diptera
粪蝇科
Sphaeroceridae
Pteremis fenestralis,
Puncticorpus cribratum
低纬度和高温 杂食性 [78]
啮虫目
Psocoptera
窃虫科Trogiidae 缘斑圆啮虫
Psoquilla marginepunctata
高密度 杂食性 [79]
等翅目
Isoptera
鼻白蚁科
Rhinotermitidae
黄胸散白蚁
Reticulitermes speratus
保幼激素水平低 杂食性 [80]
缨翅目
Thysanoptera
管蓟马科
Phlaeothripidae
管蓟马Hoplothrips karnyi 不详 植食性 [81]
蓟马科Thripidae 烟草褐花蓟马Frankliniella fusca 高温 植食性 [82]
膜翅目
Hymenoptera
姬小蜂科Eulophidae 蜾蠃巨柄姬小蜂Melittobia
digitata
、澳洲巨柄姬小蜂
M. australica
幼虫期高密度、营养短缺 寄生性 [12, 13, 22, 37]
肿腿蜂科Bethylidae 仓甲肿腿蜂Cephalonomia
gallicola
、西高止凶肿腿蜂
Apenesia sahyadrica、管氏肿腿蜂
Sclerodermus guani、川硬皮肿
腿蜂S. sichuanensis、白蜡吉丁肿
腿蜂S. pupariae
不详 寄生性 [14, 15, 16, 17, 18, 19, 20]
赤眼蜂科 Trichogrammatidae 泥蛉赤眼蜂Trichogramma
tajimaense
,毒蛾赤眼蜂
T. kurosuae,显棒赤眼蜂
T. semblidis
不详 寄生性 [21]
姬蜂科 Ichneumonoidae 沟姬蜂Gelis corruptor 充足的食物 寄生性 [83]
蚁科Formicidae 心结蚁Cardiocondyla batesii 不详 杂食性 [84, 85]
1 昆虫翅多型现象的进化适应

昆虫种内的翅型分化常见的有长翅型和短翅型、或有翅型和无翅型,其中长翅型或有翅型能飞行,而短翅型或无翅型不能飞行。目前的相关研究报道主要集中在植食性昆虫中,其中对蚜虫、飞虱、蟋蟀、长蝽等种类的研究最多。一般认为翅多型的产生是昆虫应对环境变化中在种群飞行扩散和繁殖能力之间权衡的一种生态对策。当本地环境相对稳定,有利于繁殖时,昆虫个体可通过分配更多资源用于繁殖而不是扩散,实现最高适合度。而当本地生存环境质量下降时,昆虫投入到扩散型表型中的资源将增加[5]

Roff对22种翅多型性昆虫生活史特征的分析结果表明,短翅型比长翅型的繁殖力更高,产卵时间更早[2]。翅二型的进化具有遗传基础,翅形态的高遗传力可能部分是因为拮抗基因多效性而得以保持。在二型性物种中,通常认为有翅型是迁移型,但有翅型个体的比例与具有飞行肌的有翅型个体的比例,以及这些个体的飞行习性之间,在种内和种间均存在显著的相互关系。这表明有翅型个体的比例和有翅型的迁移习性在生理和种群水平上均存在密切的相互关联[6]。翅二型昆虫的进化要求翅发育抑制激素引起的繁殖力升高,以及翅和飞行肌的产生受抑制的阈值水平发生改变。蚜虫中有翅个体与无翅个体相比发育更慢、繁殖力更低。麦长管蚜(Sitobion avenae)无翅型具有更高的体重生物量,生物量与寄主植物所含有的化学防御物质异羟肟酸(hydroxamic acids)的水平成正比。有翅蚜以降低个体大小为代价,在发育早期获得了飞行结构[7]。沙蟋(Gryllus firmus)长翅型雌性因维持飞行器官组织需要相应地提高呼吸代谢作用而消耗能量,因而产卵量受到抑制[8]。四纹豆象(Callosobruchus maculatus)短翅型雌虫产卵更早,产卵量更多,后代幼虫发育更快,死亡更早[9]。东方蝼蛄(Gryllotalpa orientalis)在5月孵化的种群9—10月份变为短翅型成虫并以成虫越冬,而6—7月份孵化的种群则以幼虫越冬,并在次年6月发育成长翅型成虫[10]。长颚斗蟋(Velarifictorus asperses)飞行肌与生殖系统的发育之间存在资源分配的权衡关系,这种资源分配的差异可能导致长翅型与短翅型个体在生活史策略上出现分化,长翅型个体具有飞行能力,而短翅型个体则在生殖方面获得更高的收益[11]

关于寄生蜂翅多型性的研究报道极少,目前仅见于姬小蜂科(Hymenoptera:Eulophidae)的蜾蠃巨柄姬小蜂(Melittobia digitata)和澳洲巨柄姬小蜂(M. australica)[12, 13],以及肿腿蜂科(Hymenoptera:Bethylidae)内的少数几种寄生蜂,如仓甲肿腿蜂(Cephalonomia gallicola)[14]、西高止凶肿腿蜂(Apenesia sahyadrica)[15]、管氏肿腿蜂(Sclerodermus guani)[16, 17]、川硬皮肿腿蜂(S. sichuanensis)[18, 19]白蜡吉丁肿腿蜂(S. pupariae)[20]。Yashiro 等报道泥蛉赤眼蜂(Trichogramma tajimaense)和毒蛾赤眼蜂(T. kurosuae)雄性均具有翅多型性(长翅型、短翅型和无翅型),显棒赤眼蜂(T. semblidis)具有翅二型性(有翅型和无翅型),其中96%的泥蛉赤眼蜂(T. tajimaense) 雄性无飞行能力,50%的毒蛾赤眼蜂(T. kurosuae)雄性不能飞行[21]。寄生泥蛉(Sialis melania)卵所发育的几乎所有显棒赤眼蜂(T. semblidis)雄性均为无翅型[21]。文献只是简单记载了这些寄生蜂种内存在翅二型现象,至于寄生蜂翅型分化的机制则未见深入研究。仅Cnsoli 和 Vinson提到寄生蜂幼虫期的密度和营养状况可能是诱导不同翅型后代发育的原因,这种形态上的变异可能是对寄主资源开发最大化和栖境移殖之间权衡的适应[12, 22]

2 昆虫翅型分化的影响因素

遗传因素和很多环境因素均对表型变异起到作用。进化和发育生物学的研究使基因对形态的贡献容易理解,但环境因素对表型的发育影响机制却知之甚少。事实上有关性状变异在环境和遗传控制之间的进化转变是如何实现的尚不清楚。朱道弘对昆虫翅多型现象及其产生机理进行了综述[23]。Roff认为在异质环境中适合度的时空变异使昆虫翅二型的遗传多态性得以维持[24]。Braendle 等指出有翅蚜的产生是为了适应种群扩散,无翅蚜是为了种群繁殖最大化[25]。苜蓿叶象甲(Hypera postica)翅型分化受多个因子调控,亲本组合、温度、幼虫密度以及寄主质量等因素均有一定影响[26]。蚜虫的雄性翅型分化是由基因控制的,而孤雌生殖的雌蚜翅型分化是环境决定的。很多因素影响雌蚜在孤雌生殖过程中翅的非遗传多型性的表达,如种群密度、寄主植物质量、温度、光周期、报警信息素、及其与捕食者、寄生物、共生生物、病原菌和内共生菌之间的相互作用等[25, 27]

2.1 遗传因素

基因型对昆虫形态决定具有显著影响,有翅类昆虫反映了扩散所带来的利益与代价之间的权衡。关于沙蟋(G. firmus)的研究结果表明,提高繁殖力的选择将导致长翅型比例降低,降低繁殖力的选择则相应地提高后代有翅型雌性的比例。这证明昆虫种群对繁殖力和翅型分化的权衡具有遗传学基础[28]。钻形蚱(Tetrix subulata)种群或家系间的变化主要受遗传控制,母代发育条件、饲养密度、个体生长率等可塑性的影响并不重要。其长翅型在种群间和种群内的变异频率可能反映了由表型和栖境决定的迁入和迁出导致的空间分选所驱动的进化修饰[29]。南方地蟋(Allonemobius socius)的翅型分化与繁殖力之间存在显著的表型负相关,且两种翅型和特定年龄的繁殖力具有明显的可遗传性。但繁殖力没有根据翅型分化为两个明显不同的类型,因而最好描述为一种基于连续分布特征的阀值作用[30]。基因型对东南田蟋(G. rubens)雌性的影响比雄性更强烈,长翅型的飞行可能进一步弱化了其繁殖能力[31]。白背飞虱(Sogatella furcifera)翅多型现象是多基因控制下的一种阈值特征,雌性有翅率受若虫期密度的影响最大,由对若虫期密度的阈值反应所决定[32]。Aukema 等认为黑通缘步甲(Pterostichus melanarius)的翅二型性也是遗传控制的[33]。翅的有无可由单一位点、两对等位基因或多基因遗传控制。这些遗传类型均可由一个通用的阈值模型进行描述,种群中短翅型频率上升可能是由于这种翅型的相对适合度的上升或长翅型的迁出所造成的[2]。Sack 和 Stern认为产生有翅雄蚜的好处可能是增加远系繁殖,雄性有翅蚜能获得更多交配机会[34]。雄性甘蔗长蝽(Cavelerius saccharivorus)翅多型性的进化可能受雌雄翅退化带来的适合度利益以及两性间的遗传相关性共同影响[35]

Brisson 等鉴定了豌豆蚜(Acyrthosiphon pisum)翅发育基因(与果蝇(Drosophila)相同),这些基因能根据不同的环境条件发育出有翅或无翅的成虫[36]。他们发现在果蝇中研究的与翅发育相关的主要基因在豆蚜基因组中均存在,而且无翅基因(apterous)和表皮生物基因(decapentaplegic)出现复制。对11种发育基因在胚胎发育和若虫跨龄时期的表达水平的研究表明,其中6个基因表现出明显的阶段特异性表达效应,而无翅基因(apterous1)在有翅型和无翅型中的表达水平表现出显著差异。可能该基因的作用近似地实现了多向性发育结果[36]

蜾蠃巨柄姬小蜂(M. digitata)雌蜂在翅的发育过程中也存在翅二型现象,并且这种表型差异的产生是由于基因差异表达的结果[37]。另外,对该寄生蜂不同翅型雌蜂的生物学研究表明,长翅型和短翅型的雌蜂在生物学习性上也有所不同。其中长翅型雌蜂为卵育型,有强烈的趋光性和扩散能力,而短翅型雌蜂为卵熟型,趋光性很弱,扩散能力很低。不同翅型雌蜂在生殖特征和扩散能力方面的差异反映了个体间由于翅型分化所产生的生活史特征的权衡[22]

2.2 非遗传因素

外界环境条件包括环境温度、光周期、食物质量、自身密度等也对昆虫翅型的发育结果产生重要的影响,称为翅的非遗传多型性。非遗传多型性是指同一基因型产生两种或多种明显不同的表现型的现象[5]。此外,平衡飞行和繁殖能力的发育调控也起着重要的作用[38]。许多蚜虫种类表现出翅多型性,翅和飞行肌的发育通常认为是以降低生殖能力为代价的。豌豆修尾蚜(Megoura crassicauda)非遗传翅多型性胚胎形成的发育调节机制可能就是补偿其翅发育所造成的生殖延迟的一种适应[39]。麦二叉蚜(Schizaphis graminum)有翅型的产生受自身密度的影响最大,其次是光周期、寄主植物和温度等因素[40]。本文对影响昆虫翅发育的各类外界因素进行了总结(表 1),但未包括因性二型性所产生的翅型差异。

麦小长蝽(Nysius huttoni)成虫种群由94.1%的长翅型、5.5%的亚短翅和0.4%的短翅型组成,低温(15 ℃)、高温(35 ℃)和短光周期低温下会加速亚短翅型和短翅型产生,而在长光周期下的高温条件则产生长翅型比例多[41]。道氏广肩水黾(Microvelia douglasi)长翅型比例受到密度、温度、光周期和食物的显著影响[42]。季节性的气候变化、种群密度及其相互作用是决定南方地蟋(A. socius)后代翅型分化的主要因素[43]。若虫阶段所经历的环境因子如高温、长日照和拥挤刺激了高粱长蝽(Dimorphopterus japonicus)长翅型的产生,而且长翅型的发生随着温度、光周期和密度的提高而升高。季节因子如气温和光周期对昆虫翅型的影响可能说明翅二型性正是昆虫对季节变化的适应策略[44]。美国山魁姬螽(Metrioptera roeselii) 长翅率与其密度强烈正相关,与植被结构和栖境湿度无关,长翅种群密度显著高于短翅种群。密度与孵化期干热天气条件正相关,在高纬度地区长翅型及其分布范围间接与天气驱动的种群变化有关[58]

褐飞虱(Nilaparvata lugens)翅型分化受光周期的影响显著,短日照下长翅型多,长日照下短翅型多[54],但也有研究认为短日照诱导更多的短翅型雄性后代产生[55]。带纹地蟋(A. fasciatus)不同地理种群间长翅型的发生比例存在显著差异[86]。先地红蝽(Pyrrhocoris sibiricus)长翅型成虫的产生具有季节性变化,在入秋初期最高[74]。Socha研究发现决定始红蝽(P. apterus)翅长度的临界光周期具有纬度梯度[87]。南部长蝽(Blissus insularis)种群密度在夏—秋季显著高于冬—春季,长翅型的比例也是在夏—秋季显著高于冬—春季,长翅型数量与种群密度成正比[73]。虽然甘蔗长蝽(Cavelerius saccharivorus)长翅型的产生是密度制约的,同时也受到季节因子的强烈影响,长日照和高温条件下长翅型后代的比例显著增加。长翅型在夏末至初秋比例最高,这些长翅型更活跃,扩散到更合适的生境如夏季种植的甘蔗地中,并从秋季到仲冬在其中产下滞育卵。成虫翅多型性和卵滞育强度属于两头下注对策,以适应亚热带冬季气候[71]。Nakao和Chikamori研究发现烟草褐花蓟马(Frankliniella fusca) 的翅型分化与光周期的关系不大,主要受到温度的控制,温度越高有翅型的比例越高[82]

豌豆蚜(A. pisum)在低密度时产生无翅蚜,高密度时产生有翅蚜。翅型分化是蚜虫种群繁殖与扩散的权衡结果[45]。饲养条件下若虫期高温、长日照和拥挤将导致高粱长蝽(D. japonicus)长翅型后代的产生。田间条件下,若虫期的密度是决定其后代翅型比例的一个关键因素,这是逃离拥挤种群的对策之一[72]。Clark等研究揭示了营养条件对沙蟋(G. firmus)种群在扩散和繁殖之间权衡的影响机制,扩散型个体的产生与增强的饮食选择密切相关,营养促进了飞行能量(脂类)的贮备,营养调控途径补充了形成这种权衡的代谢机制[63]。Hardie和Leckstein指出蚜虫翅的发育最有可能与营养削弱导致的共生体丧失有关[88]。Higashi和Bressan发现在感染了玉米花叶病毒的老玉米叶上产生长翅型玉米花翅飞虱(Peregrinus maidis)的比例显著高于年龄相近的健康叶片,表明植物病毒增加了媒介昆虫有翅型个体的产生,影响了其种群的扩散[89]。杀虫剂的使用所导致的生存环境下降对有翅蚜的产生有明显的促进影响[51]。当栖境中有天敌存在时同样也会诱导豌豆蚜(A. pisum)产生更多的有翅后代,而当共生栖境中有蚂蚁存在时这种现象便会受到一定的抑制[25]

沙蟋(G. firmus)发育过程中保幼激素酯酶活性的变化对调节血淋巴中的保幼激素水平从而影响翅型的分化具有重要的生理作用[64]。东南田蟋(G. rubens)最后2个龄期的若虫体内保幼激素III生物合成速率在同一性别不同翅型之间没有显著差异,这是因为生物合成的停止而不是保幼激素酯酶活性的升高导致了末龄初期保幼激素水平的急剧下降,可能正是这种下降启动了变态发育[90]。Zera 和 Tanaka认为保幼激素在决定曲脉姬蟋(Modicogryllus confirmatus)翅型发育的过程中可能起到一定的作用[68]。但也有相反的报道,Schwartzberg 等发现保幼激素滴度与豌豆蚜(A. pisum)有翅型后代的产生无关[91]。早熟素对昆虫的发育具有显著的影响,特别是能够诱导咽侧体细胞产生特殊的破坏因而阻止保幼激素的合成。也有研究认为早熟素对昆虫个体形态发育的影响应该是由于其所介导的拒食行为引起的[92]。由于保幼激素对昆虫具有广泛的生理调控作用,从变态到生殖,早熟素的影响也是多样的。据报道保幼激素滴度较高时可诱导蚜虫产生无翅型成虫,而在滴度较低时则促进翅的发育。研究表明,促进翅发育的化合物对翅的抑制并不是很有效[93]。早熟素处理褐飞虱(N. lugens)若虫可诱导产生长翅型成虫[94]。棉蚜(Aphis gossypii)有翅型和无翅型之间存在显著的生理差异。在成虫羽化12h内棉蚜有翅型体内总脂类、甘油三酯、游离脂肪酸的含量均显著高于无翅型。在4龄若虫至成虫期无翅型比有翅型含有更多的糖原,无翅型3—4龄若虫期海藻糖的含量明显高于有翅型,但在成虫羽化后12h情况相反。可溶性蛋白质的含量从若虫期至成虫期升高,成虫期无翅蚜高于有翅蚜,成虫期12h体内总水分含量无翅蚜显著高于有翅蚜[95]

2.3 基因型与环境影响的相互作用

遗传和环境因素均对表型变异起作用,有些蚜虫种类的生活循环中翅型决定在环境敏感(非遗传多型)和遗传控制(多态性)之间交替转变。因此,分子遗传学在理解翅多型现象的遗传控制上可能是唯一的途径,不仅可解释非遗传多型性的分子基础,也可以比较类似二型性的环境与遗传控制的机制[96]

很多非遗传多型性现象是适应表型可塑性的例子,即单一的基因型因应对环境因素而产生截然不同的表现型后代。研究发现遗传关联因子控制豌豆蚜(A. pisum)雌性翅的非遗传多型性和雄性翅多型性,这表明与环境相互作用的单一等位基因位点的基因型可以解释环境相关的翅非遗传多型性的遗传变异[97]。即使处在相同的环境条件下,不同无性系的豌豆蚜和一些其它蚜虫种类在产生有翅雌性后代的习性上也会发生变异。目前还不清楚这种遗传变异是否是昆虫为了适应环境条件的可塑性反应,有些变异可能与蚜虫对寄主植物的偏好有关,不过在同一寄主植物上仍然可观察到变异的发生[25]。Brisson等发现豌豆蚜非遗传多型性和遗传多型性之间不仅存在相似的生理差异,而且雄性和雌性一样也具有繁殖与扩散的权衡,这种权衡反映在转录表达水平上和可能的全基因组基因调控模式上[45]

Ogawa和Miura提出豌豆蚜飞行器官的发育受到胚胎期和若虫初龄期的2个发育开关点调控,由于不同的表现型存在多个发育轨迹,他们认为发育通道导致的不同翅型是在选择压力下独立进化获得的[98]。对蚂蚁翅非遗传多型性的研究表明,基因网络中有数种基因在有翅型中是保守的,而在无翅型中这些中断的位点易发生进化。同步进化的能力和保守性在蚂蚁翅发育中起着重要作用,这可能也是植物和动物中非遗传发育和进化的一种普遍特性[84]。豌豆蚜翅多型性是飞行能力与其它能力权衡的结果,豌豆蚜具有2种类型的翅多型性,雄性的翅多型性由遗传控制,胎生雌蚜的翅多型性则由环境诱导。雄性和雌性的翅多型性由不同的调节系统控制飞行器官的发育,这可能是对不同选择压力不同的适应结果[99]。白背飞虱长、短翅型的分化既由基因控制,又受外界环境因子的影响,短日照有利于白背飞虱短翅型雄虫的发生,寄主营养决定了翅型分化的方向[100]

除了日照长短和温度影响水黾(Aquarius najas)翅的发育之外,关于翅发育的表型可塑性似乎还存在遗传控制的因素,实验室条件下,无翅型个体的越冬存活率更高,生存代价解释了为什么有翅个体在北部种群更低,是为了有效适应越冬极端气候[75]

生物经常对寄生或捕食作用的危险上升表现出隔代表型变化。红秋麒麟蚜(Uroleucon nigrotuberculatum)在天敌七星瓢虫(Coccinella septempunctata)和蚜茧蜂(Aphidius polygonaphis )搜索过的寄主植物叶片上产生更高比例的有翅型后代[50]。豌豆蚜为应对寄生蜂或捕食者释放的报警信息素可能改变其隔代表现型的表达,因而影响蚜虫-天敌的种群动态[101]

3 结语

非遗传多型性是昆虫在地球上获得成功的一个主要原因,这种特性使昆虫能有效利用相同基因组,采取不同的表现型以最好地适应可预测的环境变化,或者所谓的“可预见的不可预知的”环境变化,如过度拥挤之后生存环境的恶化等[5]。虽然人们早就知道环境对昆虫翅型分化具有影响,但是如何检测这些影响,以及如何诱发不同表现型反应途径的启动至今仍未解决。功能基因组学和表观遗传学的研究发展将有助于揭示昆虫非遗传多型性的环境因素与发育过程的关系。但是基因组学技术仍需要与恰当的实验设计以及富有经验的表型分析水平相结合才可能发挥应有的作用。毫无疑问,基因组学方法可用于建立关于何种基因在不同的表现型发育过程中起作用的假说上,但是建立基因表达可塑性的因果关系仍然是一个重大挑战[5]

影响扩散进化的生态因子与翅型决定的生理基础的关系也是研究的难点。Zera和Denno指出对翅二型昆虫的研究在我们理解昆虫扩散、生活史和性状多态性的生态学、进化和生理学发展方面将起着关键作用[38]。环境因子可在多大程度上影响飞行能力与繁殖能力之间的权衡,雄性个体通过交配系统对这种权衡的作用也有必要进行研究。此外,激素和内分泌作用机制也还需要深入探讨。翅型分化可以看作是环境敏感开关决定昆虫发育成有翅/长翅型或无翅/短翅型,这种开关对环境因素的敏感性可由多基因或单基因控制。保证个体发育成特定翅型的开关可能在某个特殊的发育敏感时期起作用,包括胚胎期(出生前控制)、幼虫早期(出生后控制)以及幼虫末龄控制。在更宽泛的生物水平上,非遗传多型性对诸如物种形成速率和表型多样性现象的影响是一个研究热点[102]

另外,表观遗传调控机制如DNA甲基化作用越来越多地用于昆虫非遗传多型性研究中,但这些DNA甲基化作用与其他DNA修饰机制之间的相互作用,以及对转录、转录后和翻译活动的调节等仍不清楚。非遗传多型性如何在不同层次的生物组织中演化及其结果如何等仍需要进一步研究。促进非遗传多型性特性从单一表型状态进化的基因变化类型至今仍未很好的建立起来,可能包括控制发育活动的细微变化,如阈值、敏感水平和时间节奏的调节等。有针对性的比较研究具有和不具有非遗传多型性的相近物种可能揭示这些问题[5]。雌性翅的非遗传多型性与雄性翅的遗传多态性的翅的表现型极为相似,与非遗传多型性相关的表现型和环境之间的相互作用可能涉及到与控制遗传多型性相同的基因位点。翅的非遗传多型性是一个明显的适应性表型可塑性的例子,雌性翅的非遗传多型性与雄性翅的遗传多型性的共表达为研究环境与遗传诱导的可变表型提供了良好的材料,这有助于弄清遗传因子和环境因子是如何交替控制同一发育结果,以及这种非遗传多型性与遗传多型性之间的进化转换是如何发生的[25]。 控制表型多态性相关基因的鉴定,可能会促进非遗传多型性所产生的相似的表型变化机制的研究。迄今已有多个与昆虫翅发育相关的基因获得鉴定[103, 104]。目前对遗传和发育引起的不同表现型的表达机制仍知之不多,基因组学的研究必将为揭示昆虫翅多型现象的内在机制提供全新的机遇[25]

迄今所涉及的翅多型现象研究对象绝大多数为植食性昆虫,而对控制害虫的天敌寄生蜂的翅型分化研究鲜见报道。目前我国在林业害虫生物防治中广泛应用的几种肿腿蜂均具有翅二型现象,雄性基本有翅而雌性大多数无翅,其中管氏肿腿蜂(Sclerodermus guani)和川硬皮肿腿蜂(S. sichuanensis)均有无翅型和有翅型2种个体,雌性主要为无翅型,有翅雌性较少见,而雄性则基本为有翅型,无翅雄性极难见到[16, 17, 18, 19]。白蜡吉丁肿腿蜂(S. pupariae)是近年来发现的一个肿腿蜂新种[105],自然条件下寄生白蜡窄吉丁(Agrilus planipennis)蛹,后来发现也能寄生该害虫的幼虫和危害白蜡树的咖啡虎天牛(Xylotrechus grayii)幼虫[106]。进一步的生物学研究表明,该蜂可成功寄生柑桔窄吉丁(A. auriventris)、苹小吉丁(A. mali)、花椒窄吉丁A. zanthoxylumi、核桃脊胸纹吉丁Nalanda sp.、复纹狭天牛(Stenhomalus complicatus)、光肩星天牛(Anoplophora glabripennis)、栗山天牛(Massicus raddei)、松褐天牛(Monochamus alternatus)、麻天牛(Thyestilla gebleri)等多种吉丁甲和天牛的幼虫,且后代均能正常完成生长发育,是一种非常优良的蛀干害虫天敌[20, 107]。白蜡吉丁肿腿蜂以成虫越冬,自然种群越冬后成虫所产的第1代后代中雌性有翅率较高,平均可达56.6%,第2代则降低到14.7%,此后世代中雌性大多为无翅型。雄性个体比例较低,约占2%—5%,且雄性基本均为有翅型[20]。这几种肿腿蜂在我国林业上广泛用于防治天牛和吉丁虫等重要蛀干类害虫,已实现工厂化人工大量繁育,但由于繁殖出的雌性基本为无翅型个体,因此释放后其扩散能力受到限制,只能依靠爬行扩散,从而影响了生物防治效果,也给生产应用上带来了不便,在人工放蜂时需将寄生蜂人为释放到有寄主害虫的树干上,以帮助寄生蜂寻找寄主。因此,如果能明确肿腿蜂发育过程中翅型分化的机制,通过人为干预,培养出较高比例的有翅型雌蜂,释放后有利于种群的自然扩散,提高生物防治效果,将在指导人工大量繁殖高品质的寄生蜂个体用于生产防治上具有重要的指导意义和应用价值。

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