昆蟲翅型分化的表型可塑性機(jī)制

王小藝, 楊忠岐, 魏 可, 唐艷龍

中國林業(yè)科學(xué)研究院森林生態(tài)環(huán)境與保護(hù)研究所, 國家林業(yè)局森林保護(hù)學(xué)重點(diǎn)實(shí)驗(yàn)室, 北京 100091

昆蟲翅型分化的表型可塑性機(jī)制

王小藝, 楊忠岐*, 魏 可, 唐艷龍

中國林業(yè)科學(xué)研究院森林生態(tài)環(huán)境與保護(hù)研究所, 國家林業(yè)局森林保護(hù)學(xué)重點(diǎn)實(shí)驗(yàn)室, 北京 100091

翅多型現(xiàn)象在昆蟲中廣泛存在，是昆蟲在飛行擴(kuò)散和繁殖能力之間權(quán)衡的一種策略，對(duì)種群的環(huán)境適應(yīng)性進(jìn)化具有重要的意義。目前在植食性昆蟲中研究較多，有關(guān)寄生蜂的翅型分化鮮見報(bào)道。綜述了昆蟲翅型分化的表型可塑性機(jī)制。遺傳因素和環(huán)境因素均對(duì)昆蟲翅的發(fā)育產(chǎn)生影響，基因型對(duì)翅型的決定具有顯著作用，外界環(huán)境條件，包括溫度、光周期、食物質(zhì)量、自身密度、外源激素等因素對(duì)昆蟲翅的發(fā)育也產(chǎn)生重要的調(diào)節(jié)作用，從而產(chǎn)生翅的非遺傳多型性現(xiàn)象。此外，天敵的寄生或捕食作用可能會(huì)誘導(dǎo)某些昆蟲的翅型產(chǎn)生隔代表型變化。對(duì)昆蟲產(chǎn)生翅多型現(xiàn)象的生態(tài)學(xué)意義及其在生物進(jìn)化過程中的作用進(jìn)行了討論，并探討了寄生性昆蟲翅型分化機(jī)制在生物防治上的可能應(yīng)用途徑。功能基因組學(xué)和表觀遺傳學(xué)的進(jìn)一步發(fā)展可望為徹底揭示昆蟲翅型分化機(jī)制提供新的機(jī)遇和技術(shù)手段。

翅多型性; 非遺傳多型性; 表型可塑性; 適應(yīng)性進(jìn)化

表型可塑性是指同一基因型因受不同的環(huán)境影響而產(chǎn)生不同表現(xiàn)型的現(xiàn)象[1]，是生物對(duì)環(huán)境變化的一種適應(yīng)。昆蟲的翅多型現(xiàn)象在同翅目、半翅目、鞘翅目、膜翅目、直翅目、雙翅目、鱗翅目、等翅目、嚙蟲目以及革翅目中廣泛存在(表1)，這對(duì)種群的適應(yīng)性具有十分重要的意義。因?yàn)榫叱嵝涂梢赃h(yuǎn)距離擴(kuò)散、找到更合適的棲境供后代生存和繁衍。翅二型性昆蟲是研究擴(kuò)散進(jìn)化的優(yōu)良材料，翅的二型性是昆蟲在飛行能力和繁殖能力之間權(quán)衡的一種策略，但種群保持翅型分化的機(jī)制目前仍不清楚。通常認(rèn)為遺傳基因和環(huán)境因素均對(duì)昆蟲翅型的決定產(chǎn)生影響[2- 4]。本文總結(jié)了昆蟲翅型分化的表型可塑性機(jī)制，以期指導(dǎo)寄生性天敵昆蟲在生物防治上的有效利用。

表1 具有翅型分化特性的昆蟲類別及影響翅生長發(fā)育的主要因素Table 1 Insects with wing dimorphism and major impact factors of wing development

本表不包括因性二型性所產(chǎn)生的翅型差異

1 昆蟲翅多型現(xiàn)象的進(jìn)化適應(yīng)

昆蟲種內(nèi)的翅型分化常見的有長翅型和短翅型、或有翅型和無翅型，其中長翅型或有翅型能飛行，而短翅型或無翅型不能飛行。目前的相關(guān)研究報(bào)道主要集中在植食性昆蟲中，其中對(duì)蚜蟲、飛虱、蟋蟀、長蝽等種類的研究最多。一般認(rèn)為翅多型的產(chǎn)生是昆蟲應(yīng)對(duì)環(huán)境變化中在種群飛行擴(kuò)散和繁殖能力之間權(quán)衡的一種生態(tài)對(duì)策。當(dāng)本地環(huán)境相對(duì)穩(wěn)定，有利于繁殖時(shí)，昆蟲個(gè)體可通過分配更多資源用于繁殖而不是擴(kuò)散，實(shí)現(xiàn)最高適合度。而當(dāng)本地生存環(huán)境質(zhì)量下降時(shí)，昆蟲投入到擴(kuò)散型表型中的資源將增加[5]。

Roff對(duì)22種翅多型性昆蟲生活史特征的分析結(jié)果表明，短翅型比長翅型的繁殖力更高，產(chǎn)卵時(shí)間更早[2]。翅二型的進(jìn)化具有遺傳基礎(chǔ)，翅形態(tài)的高遺傳力可能部分是因?yàn)檗卓够蚨嘈远靡员３帧Ｔ诙托晕锓N中，通常認(rèn)為有翅型是遷移型，但有翅型個(gè)體的比例與具有飛行肌的有翅型個(gè)體的比例，以及這些個(gè)體的飛行習(xí)性之間，在種內(nèi)和種間均存在顯著的相互關(guān)系。這表明有翅型個(gè)體的比例和有翅型的遷移習(xí)性在生理和種群水平上均存在密切的相互關(guān)聯(lián)[6]。翅二型昆蟲的進(jìn)化要求翅發(fā)育抑制激素引起的繁殖力升高，以及翅和飛行肌的產(chǎn)生受抑制的閾值水平發(fā)生改變。蚜蟲中有翅個(gè)體與無翅個(gè)體相比發(fā)育更慢、繁殖力更低。麥長管蚜(Sitobionavenae)無翅型具有更高的體重生物量，生物量與寄主植物所含有的化學(xué)防御物質(zhì)異羥肟酸(hydroxamic acids)的水平成正比。有翅蚜以降低個(gè)體大小為代價(jià)，在發(fā)育早期獲得了飛行結(jié)構(gòu)[7]。沙蟋(Gryllusfirmus)長翅型雌性因維持飛行器官組織需要相應(yīng)地提高呼吸代謝作用而消耗能量，因而產(chǎn)卵量受到抑制[8]。四紋豆象(Callosobruchusmaculatus)短翅型雌蟲產(chǎn)卵更早，產(chǎn)卵量更多，后代幼蟲發(fā)育更快，死亡更早[9]。東方螻蛄(Gryllotalpaorientalis)在5月孵化的種群9—10月份變?yōu)槎坛嵝统上x并以成蟲越冬，而6—7月份孵化的種群則以幼蟲越冬，并在次年6月發(fā)育成長翅型成蟲[10]。長顎斗蟋(Velarifictorusasperses)飛行肌與生殖系統(tǒng)的發(fā)育之間存在資源分配的權(quán)衡關(guān)系，這種資源分配的差異可能導(dǎo)致長翅型與短翅型個(gè)體在生活史策略上出現(xiàn)分化，長翅型個(gè)體具有飛行能力，而短翅型個(gè)體則在生殖方面獲得更高的收益[11]。

關(guān)于寄生蜂翅多型性的研究報(bào)道極少，目前僅見于姬小蜂科(Hymenoptera：Eulophidae)的蜾蠃巨柄姬小蜂(Melittobiadigitata)和澳洲巨柄姬小蜂(M.australica)[12-13]，以及腫腿蜂科(Hymenoptera：Bethylidae)內(nèi)的少數(shù)幾種寄生蜂，如倉甲腫腿蜂(Cephalonomiagallicola)[14]、西高止兇腫腿蜂(Apenesiasahyadrica)[15]、管氏腫腿蜂(Sclerodermusguani)[16-17]、川硬皮腫腿蜂(S.sichuanensis)[18-19]、白蠟吉丁腫腿蜂(S.pupariae)[20]。Yashiro 等報(bào)道泥蛉赤眼蜂(Trichogrammatajimaense)和毒蛾赤眼蜂(T.kurosuae)雄性均具有翅多型性(長翅型、短翅型和無翅型)，顯棒赤眼蜂(T.semblidis)具有翅二型性(有翅型和無翅型)，其中96%的泥蛉赤眼蜂(T.tajimaense) 雄性無飛行能力，50%的毒蛾赤眼蜂(T.kurosuae)雄性不能飛行[21]。寄生泥蛉(Sialismelania)卵所發(fā)育的幾乎所有顯棒赤眼蜂(T.semblidis)雄性均為無翅型[21]。文獻(xiàn)只是簡單記載了這些寄生蜂種內(nèi)存在翅二型現(xiàn)象，至于寄生蜂翅型分化的機(jī)制則未見深入研究。僅Cnsoli 和 Vinson提到寄生蜂幼蟲期的密度和營養(yǎng)狀況可能是誘導(dǎo)不同翅型后代發(fā)育的原因，這種形態(tài)上的變異可能是對(duì)寄主資源開發(fā)最大化和棲境移殖之間權(quán)衡的適應(yīng)[12, 22]。

2 昆蟲翅型分化的影響因素

遺傳因素和很多環(huán)境因素均對(duì)表型變異起到作用。進(jìn)化和發(fā)育生物學(xué)的研究使基因?qū)π螒B(tài)的貢獻(xiàn)容易理解，但環(huán)境因素對(duì)表型的發(fā)育影響機(jī)制卻知之甚少。事實(shí)上有關(guān)性狀變異在環(huán)境和遺傳控制之間的進(jìn)化轉(zhuǎn)變是如何實(shí)現(xiàn)的尚不清楚。朱道弘對(duì)昆蟲翅多型現(xiàn)象及其產(chǎn)生機(jī)理進(jìn)行了綜述[23]。Roff認(rèn)為在異質(zhì)環(huán)境中適合度的時(shí)空變異使昆蟲翅二型的遺傳多態(tài)性得以維持[24]。Braendle 等指出有翅蚜的產(chǎn)生是為了適應(yīng)種群擴(kuò)散，無翅蚜是為了種群繁殖最大化[25]。苜蓿葉象甲(Hyperapostica)翅型分化受多個(gè)因子調(diào)控，親本組合、溫度、幼蟲密度以及寄主質(zhì)量等因素均有一定影響[26]。蚜蟲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環(huán)境決定的。很多因素影響雌蚜在孤雌生殖過程中翅的非遺傳多型性的表達(dá)，如種群密度、寄主植物質(zhì)量、溫度、光周期、報(bào)警信息素、及其與捕食者、寄生物、共生生物、病原菌和內(nèi)共生菌之間的相互作用等[25, 27]。

2.1 遺傳因素

基因型對(duì)昆蟲形態(tài)決定具有顯著影響，有翅類昆蟲反映了擴(kuò)散所帶來的利益與代價(jià)之間的權(quán)衡。關(guān)于沙蟋(G.firmus)的研究結(jié)果表明，提高繁殖力的選擇將導(dǎo)致長翅型比例降低，降低繁殖力的選擇則相應(yīng)地提高后代有翅型雌性的比例。這證明昆蟲種群對(duì)繁殖力和翅型分化的權(quán)衡具有遺傳學(xué)基礎(chǔ)[28]。鉆形蚱(Tetrixsubulata)種群或家系間的變化主要受遺傳控制，母代發(fā)育條件、飼養(yǎng)密度、個(gè)體生長率等可塑性的影響并不重要。其長翅型在種群間和種群內(nèi)的變異頻率可能反映了由表型和棲境決定的遷入和遷出導(dǎo)致的空間分選所驅(qū)動(dòng)的進(jìn)化修飾[29]。南方地蟋(Allonemobiussocius)的翅型分化與繁殖力之間存在顯著的表型負(fù)相關(guān)，且兩種翅型和特定年齡的繁殖力具有明顯的可遺傳性。但繁殖力沒有根據(jù)翅型分化為兩個(gè)明顯不同的類型，因而最好描述為一種基于連續(xù)分布特征的閥值作用[30]。基因型對(duì)東南田蟋(G.rubens)雌性的影響比雄性更強(qiáng)烈，長翅型的飛行可能進(jìn)一步弱化了其繁殖能力[31]。白背飛虱(Sogatellafurcifera)翅多型現(xiàn)象是多基因控制下的一種閾值特征，雌性有翅率受若蟲期密度的影響最大，由對(duì)若蟲期密度的閾值反應(yīng)所決定[32]。Aukema 等認(rèn)為黑通緣步甲(Pterostichusmelanarius)的翅二型性也是遺傳控制的[33]。翅的有無可由單一位點(diǎn)、兩對(duì)等位基因或多基因遺傳控制。這些遺傳類型均可由一個(gè)通用的閾值模型進(jìn)行描述，種群中短翅型頻率上升可能是由于這種翅型的相對(duì)適合度的上升或長翅型的遷出所造成的[2]。Sack 和 Stern認(rèn)為產(chǎn)生有翅雄蚜的好處可能是增加遠(yuǎn)系繁殖，雄性有翅蚜能獲得更多交配機(jī)會(huì)[34]。雄性甘蔗長蝽(Caveleriussaccharivorus)翅多型性的進(jìn)化可能受雌雄翅退化帶來的適合度利益以及兩性間的遺傳相關(guān)性共同影響[35]。

Brisson 等鑒定了豌豆蚜(Acyrthosiphonpisum)翅發(fā)育基因(與果蠅(Drosophila)相同)，這些基因能根據(jù)不同的環(huán)境條件發(fā)育出有翅或無翅的成蟲[36]。他們發(fā)現(xiàn)在果蠅中研究的與翅發(fā)育相關(guān)的主要基因在豆蚜基因組中均存在，而且無翅基因(apterous)和表皮生物基因(decapentaplegic)出現(xiàn)復(fù)制。對(duì)11種發(fā)育基因在胚胎發(fā)育和若蟲跨齡時(shí)期的表達(dá)水平的研究表明，其中6個(gè)基因表現(xiàn)出明顯的階段特異性表達(dá)效應(yīng)，而無翅基因(apterous1)在有翅型和無翅型中的表達(dá)水平表現(xiàn)出顯著差異。可能該基因的作用近似地實(shí)現(xiàn)了多向性發(fā)育結(jié)果[36]。

蜾蠃巨柄姬小蜂(M.digitata)雌蜂在翅的發(fā)育過程中也存在翅二型現(xiàn)象，并且這種表型差異的產(chǎn)生是由于基因差異表達(dá)的結(jié)果[37]。另外，對(duì)該寄生蜂不同翅型雌蜂的生物學(xué)研究表明，長翅型和短翅型的雌蜂在生物學(xué)習(xí)性上也有所不同。其中長翅型雌蜂為卵育型，有強(qiáng)烈的趨光性和擴(kuò)散能力，而短翅型雌蜂為卵熟型，趨光性很弱，擴(kuò)散能力很低。不同翅型雌蜂在生殖特征和擴(kuò)散能力方面的差異反映了個(gè)體間由于翅型分化所產(chǎn)生的生活史特征的權(quán)衡[22]。

2.2 非遺傳因素

外界環(huán)境條件包括環(huán)境溫度、光周期、食物質(zhì)量、自身密度等也對(duì)昆蟲翅型的發(fā)育結(jié)果產(chǎn)生重要的影響，稱為翅的非遺傳多型性。非遺傳多型性是指同一基因型產(chǎn)生兩種或多種明顯不同的表現(xiàn)型的現(xiàn)象[5]。此外，平衡飛行和繁殖能力的發(fā)育調(diào)控也起著重要的作用[38]。許多蚜蟲種類表現(xiàn)出翅多型性，翅和飛行肌的發(fā)育通常認(rèn)為是以降低生殖能力為代價(jià)的。豌豆修尾蚜(Megouracrassicauda)非遺傳翅多型性胚胎形成的發(fā)育調(diào)節(jié)機(jī)制可能就是補(bǔ)償其翅發(fā)育所造成的生殖延遲的一種適應(yīng)[39]。麥二叉蚜(Schizaphisgraminum)有翅型的產(chǎn)生受自身密度的影響最大，其次是光周期、寄主植物和溫度等因素[40]。本文對(duì)影響昆蟲翅發(fā)育的各類外界因素進(jìn)行了總結(jié)(表1)，但未包括因性二型性所產(chǎn)生的翅型差異。

麥小長蝽(Nysiushuttoni)成蟲種群由94.1%的長翅型、5.5%的亞短翅和0.4%的短翅型組成，低溫(15 ℃)、高溫(35 ℃)和短光周期低溫下會(huì)加速亞短翅型和短翅型產(chǎn)生，而在長光周期下的高溫條件則產(chǎn)生長翅型比例多[41]。道氏廣肩水黽(Microveliadouglasi)長翅型比例受到密度、溫度、光周期和食物的顯著影響[42]。季節(jié)性的氣候變化、種群密度及其相互作用是決定南方地蟋(A.socius)后代翅型分化的主要因素[43]。若蟲階段所經(jīng)歷的環(huán)境因子如高溫、長日照和擁擠刺激了高粱長蝽(Dimorphopterusjaponicus)長翅型的產(chǎn)生，而且長翅型的發(fā)生隨著溫度、光周期和密度的提高而升高。季節(jié)因子如氣溫和光周期對(duì)昆蟲翅型的影響可能說明翅二型性正是昆蟲對(duì)季節(jié)變化的適應(yīng)策略[44]。美國山魁姬螽(Metriopteraroeselii) 長翅率與其密度強(qiáng)烈正相關(guān)，與植被結(jié)構(gòu)和棲境濕度無關(guān)，長翅種群密度顯著高于短翅種群。密度與孵化期干熱天氣條件正相關(guān)，在高緯度地區(qū)長翅型及其分布范圍間接與天氣驅(qū)動(dòng)的種群變化有關(guān)[58]。

褐飛虱(Nilaparvatalugens)翅型分化受光周期的影響顯著，短日照下長翅型多，長日照下短翅型多[54]，但也有研究認(rèn)為短日照誘導(dǎo)更多的短翅型雄性后代產(chǎn)生[55]。帶紋地蟋(A.fasciatus)不同地理種群間長翅型的發(fā)生比例存在顯著差異[86]。先地紅蝽(Pyrrhocorissibiricus)長翅型成蟲的產(chǎn)生具有季節(jié)性變化，在入秋初期最高[74]。Socha研究發(fā)現(xiàn)決定始紅蝽(P.apterus)翅長度的臨界光周期具有緯度梯度[87]。南部長蝽(Blissusinsularis)種群密度在夏—秋季顯著高于冬—春季，長翅型的比例也是在夏—秋季顯著高于冬—春季，長翅型數(shù)量與種群密度成正比[73]。雖然甘蔗長蝽(Caveleriussaccharivorus)長翅型的產(chǎn)生是密度制約的，同時(shí)也受到季節(jié)因子的強(qiáng)烈影響，長日照和高溫條件下長翅型后代的比例顯著增加。長翅型在夏末至初秋比例最高，這些長翅型更活躍，擴(kuò)散到更合適的生境如夏季種植的甘蔗地中，并從秋季到仲冬在其中產(chǎn)下滯育卵。成蟲翅多型性和卵滯育強(qiáng)度屬于兩頭下注對(duì)策，以適應(yīng)亞熱帶冬季氣候[71]。Nakao和Chikamori研究發(fā)現(xiàn)煙草褐花薊馬(Frankliniellafusca) 的翅型分化與光周期的關(guān)系不大，主要受到溫度的控制，溫度越高有翅型的比例越高[82]。

豌豆蚜(A.pisum)在低密度時(shí)產(chǎn)生無翅蚜，高密度時(shí)產(chǎn)生有翅蚜。翅型分化是蚜蟲種群繁殖與擴(kuò)散的權(quán)衡結(jié)果[45]。飼養(yǎng)條件下若蟲期高溫、長日照和擁擠將導(dǎo)致高粱長蝽(D.japonicus)長翅型后代的產(chǎn)生。田間條件下，若蟲期的密度是決定其后代翅型比例的一個(gè)關(guān)鍵因素，這是逃離擁擠種群的對(duì)策之一[72]。Clark等研究揭示了營養(yǎng)條件對(duì)沙蟋(G.firmus)種群在擴(kuò)散和繁殖之間權(quán)衡的影響機(jī)制，擴(kuò)散型個(gè)體的產(chǎn)生與增強(qiáng)的飲食選擇密切相關(guān)，營養(yǎng)促進(jìn)了飛行能量(脂類)的貯備，營養(yǎng)調(diào)控途徑補(bǔ)充了形成這種權(quán)衡的代謝機(jī)制[63]。Hardie和Leckstein指出蚜蟲翅的發(fā)育最有可能與營養(yǎng)削弱導(dǎo)致的共生體喪失有關(guān)[88]。Higashi和Bressan發(fā)現(xiàn)在感染了玉米花葉病毒的老玉米葉上產(chǎn)生長翅型玉米花翅飛虱(Peregrinusmaidis)的比例顯著高于年齡相近的健康葉片，表明植物病毒增加了媒介昆蟲有翅型個(gè)體的產(chǎn)生，影響了其種群的擴(kuò)散[89]。殺蟲劑的使用所導(dǎo)致的生存環(huán)境下降對(duì)有翅蚜的產(chǎn)生有明顯的促進(jìn)影響[51]。當(dāng)棲境中有天敵存在時(shí)同樣也會(huì)誘導(dǎo)豌豆蚜(A.pisum)產(chǎn)生更多的有翅后代，而當(dāng)共生棲境中有螞蟻存在時(shí)這種現(xiàn)象便會(huì)受到一定的抑制[25]。

沙蟋(G.firmus)發(fā)育過程中保幼激素酯酶活性的變化對(duì)調(diào)節(jié)血淋巴中的保幼激素水平從而影響翅型的分化具有重要的生理作用[64]。東南田蟋(G.rubens)最后2個(gè)齡期的若蟲體內(nèi)保幼激素III生物合成速率在同一性別不同翅型之間沒有顯著差異，這是因?yàn)樯锖铣傻耐Ｖ苟皇潜Ｓ准に仵ッ富钚缘纳邔?dǎo)致了末齡初期保幼激素水平的急劇下降，可能正是這種下降啟動(dòng)了變態(tài)發(fā)育[90]。Zera 和 Tanaka認(rèn)為保幼激素在決定曲脈姬蟋(Modicogryllusconfirmatus)翅型發(fā)育的過程中可能起到一定的作用[68]。但也有相反的報(bào)道，Schwartzberg 等發(fā)現(xiàn)保幼激素滴度與豌豆蚜(A.pisum)有翅型后代的產(chǎn)生無關(guān)[91]。早熟素對(duì)昆蟲的發(fā)育具有顯著的影響，特別是能夠誘導(dǎo)咽側(cè)體細(xì)胞產(chǎn)生特殊的破壞因而阻止保幼激素的合成。也有研究認(rèn)為早熟素對(duì)昆蟲個(gè)體形態(tài)發(fā)育的影響應(yīng)該是由于其所介導(dǎo)的拒食行為引起的[92]。由于保幼激素對(duì)昆蟲具有廣泛的生理調(diào)控作用，從變態(tài)到生殖，早熟素的影響也是多樣的。據(jù)報(bào)道保幼激素滴度較高時(shí)可誘導(dǎo)蚜蟲產(chǎn)生無翅型成蟲，而在滴度較低時(shí)則促進(jìn)翅的發(fā)育。研究表明，促進(jìn)翅發(fā)育的化合物對(duì)翅的抑制并不是很有效[93]。早熟素處理褐飛虱(N.lugens)若蟲可誘導(dǎo)產(chǎn)生長翅型成蟲[94]。棉蚜(Aphisgossypii)有翅型和無翅型之間存在顯著的生理差異。在成蟲羽化12h內(nèi)棉蚜有翅型體內(nèi)總脂類、甘油三酯、游離脂肪酸的含量均顯著高于無翅型。在4齡若蟲至成蟲期無翅型比有翅型含有更多的糖原，無翅型3—4齡若蟲期海藻糖的含量明顯高于有翅型，但在成蟲羽化后12h情況相反。可溶性蛋白質(zhì)的含量從若蟲期至成蟲期升高，成蟲期無翅蚜高于有翅蚜，成蟲期12h體內(nèi)總水分含量無翅蚜顯著高于有翅蚜[95]。

2.3 基因型與環(huán)境影響的相互作用

遺傳和環(huán)境因素均對(duì)表型變異起作用，有些蚜蟲種類的生活循環(huán)中翅型決定在環(huán)境敏感(非遺傳多型)和遺傳控制(多態(tài)性)之間交替轉(zhuǎn)變。因此，分子遺傳學(xué)在理解翅多型現(xiàn)象的遺傳控制上可能是唯一的途徑，不僅可解釋非遺傳多型性的分子基礎(chǔ)，也可以比較類似二型性的環(huán)境與遺傳控制的機(jī)制[96]。

很多非遺傳多型性現(xiàn)象是適應(yīng)表型可塑性的例子，即單一的基因型因應(yīng)對(duì)環(huán)境因素而產(chǎn)生截然不同的表現(xiàn)型后代。研究發(fā)現(xiàn)遺傳關(guān)聯(lián)因子控制豌豆蚜(A.pisum)雌性翅的非遺傳多型性和雄性翅多型性，這表明與環(huán)境相互作用的單一等位基因位點(diǎn)的基因型可以解釋環(huán)境相關(guān)的翅非遺傳多型性的遺傳變異[97]。即使處在相同的環(huán)境條件下，不同無性系的豌豆蚜和一些其它蚜蟲種類在產(chǎn)生有翅雌性后代的習(xí)性上也會(huì)發(fā)生變異。目前還不清楚這種遺傳變異是否是昆蟲為了適應(yīng)環(huán)境條件的可塑性反應(yīng)，有些變異可能與蚜蟲對(duì)寄主植物的偏好有關(guān)，不過在同一寄主植物上仍然可觀察到變異的發(fā)生[25]。Brisson等發(fā)現(xiàn)豌豆蚜非遺傳多型性和遺傳多型性之間不僅存在相似的生理差異，而且雄性和雌性一樣也具有繁殖與擴(kuò)散的權(quán)衡，這種權(quán)衡反映在轉(zhuǎn)錄表達(dá)水平上和可能的全基因組基因調(diào)控模式上[45]。

Ogawa和Miura提出豌豆蚜飛行器官的發(fā)育受到胚胎期和若蟲初齡期的2個(gè)發(fā)育開關(guān)點(diǎn)調(diào)控，由于不同的表現(xiàn)型存在多個(gè)發(fā)育軌跡，他們認(rèn)為發(fā)育通道導(dǎo)致的不同翅型是在選擇壓力下獨(dú)立進(jìn)化獲得的[98]。對(duì)螞蟻翅非遺傳多型性的研究表明，基因網(wǎng)絡(luò)中有數(shù)種基因在有翅型中是保守的，而在無翅型中這些中斷的位點(diǎn)易發(fā)生進(jìn)化。同步進(jìn)化的能力和保守性在螞蟻翅發(fā)育中起著重要作用，這可能也是植物和動(dòng)物中非遺傳發(fā)育和進(jìn)化的一種普遍特性[84]。豌豆蚜翅多型性是飛行能力與其它能力權(quán)衡的結(jié)果，豌豆蚜具有2種類型的翅多型性，雄性的翅多型性由遺傳控制，胎生雌蚜的翅多型性則由環(huán)境誘導(dǎo)。雄性和雌性的翅多型性由不同的調(diào)節(jié)系統(tǒng)控制飛行器官的發(fā)育，這可能是對(duì)不同選擇壓力不同的適應(yīng)結(jié)果[99]。白背飛虱長、短翅型的分化既由基因控制，又受外界環(huán)境因子的影響，短日照有利于白背飛虱短翅型雄蟲的發(fā)生，寄主營養(yǎng)決定了翅型分化的方向[100]。

除了日照長短和溫度影響水黽(Aquariusnajas)翅的發(fā)育之外，關(guān)于翅發(fā)育的表型可塑性似乎還存在遺傳控制的因素，實(shí)驗(yàn)室條件下，無翅型個(gè)體的越冬存活率更高，生存代價(jià)解釋了為什么有翅個(gè)體在北部種群更低，是為了有效適應(yīng)越冬極端氣候[75]。

生物經(jīng)常對(duì)寄生或捕食作用的危險(xiǎn)上升表現(xiàn)出隔代表型變化。紅秋麒麟蚜(Uroleuconnigrotuberculatum)在天敵七星瓢蟲(Coccinellaseptempunctata)和蚜繭蜂(Aphidiuspolygonaphis)搜索過的寄主植物葉片上產(chǎn)生更高比例的有翅型后代[50]。豌豆蚜為應(yīng)對(duì)寄生蜂或捕食者釋放的報(bào)警信息素可能改變其隔代表現(xiàn)型的表達(dá)，因而影響蚜蟲-天敵的種群動(dòng)態(tài)[101]。

3 結(jié)語

非遺傳多型性是昆蟲在地球上獲得成功的一個(gè)主要原因，這種特性使昆蟲能有效利用相同基因組，采取不同的表現(xiàn)型以最好地適應(yīng)可預(yù)測(cè)的環(huán)境變化，或者所謂的“可預(yù)見的不可預(yù)知的”環(huán)境變化，如過度擁擠之后生存環(huán)境的惡化等[5]。雖然人們?cè)缇椭拉h(huán)境對(duì)昆蟲翅型分化具有影響，但是如何檢測(cè)這些影響，以及如何誘發(fā)不同表現(xiàn)型反應(yīng)途徑的啟動(dòng)至今仍未解決。功能基因組學(xué)和表觀遺傳學(xué)的研究發(fā)展將有助于揭示昆蟲非遺傳多型性的環(huán)境因素與發(fā)育過程的關(guān)系。但是基因組學(xué)技術(shù)仍需要與恰當(dāng)?shù)膶?shí)驗(yàn)設(shè)計(jì)以及富有經(jīng)驗(yàn)的表型分析水平相結(jié)合才可能發(fā)揮應(yīng)有的作用。毫無疑問，基因組學(xué)方法可用于建立關(guān)于何種基因在不同的表現(xiàn)型發(fā)育過程中起作用的假說上，但是建立基因表達(dá)可塑性的因果關(guān)系仍然是一個(gè)重大挑戰(zhàn)[5]。

影響擴(kuò)散進(jìn)化的生態(tài)因子與翅型決定的生理基礎(chǔ)的關(guān)系也是研究的難點(diǎn)。Zera和Denno指出對(duì)翅二型昆蟲的研究在我們理解昆蟲擴(kuò)散、生活史和性狀多態(tài)性的生態(tài)學(xué)、進(jìn)化和生理學(xué)發(fā)展方面將起著關(guān)鍵作用[38]。環(huán)境因子可在多大程度上影響飛行能力與繁殖能力之間的權(quán)衡，雄性個(gè)體通過交配系統(tǒng)對(duì)這種權(quán)衡的作用也有必要進(jìn)行研究。此外，激素和內(nèi)分泌作用機(jī)制也還需要深入探討。翅型分化可以看作是環(huán)境敏感開關(guān)決定昆蟲發(fā)育成有翅/長翅型或無翅/短翅型，這種開關(guān)對(duì)環(huán)境因素的敏感性可由多基因或單基因控制。保證個(gè)體發(fā)育成特定翅型的開關(guān)可能在某個(gè)特殊的發(fā)育敏感時(shí)期起作用，包括胚胎期(出生前控制)、幼蟲早期(出生后控制)以及幼蟲末齡控制。在更寬泛的生物水平上，非遺傳多型性對(duì)諸如物種形成速率和表型多樣性現(xiàn)象的影響是一個(gè)研究熱點(diǎn)[102]。

另外，表觀遺傳調(diào)控機(jī)制如DNA甲基化作用越來越多地用于昆蟲非遺傳多型性研究中，但這些DNA甲基化作用與其他DNA修飾機(jī)制之間的相互作用，以及對(duì)轉(zhuǎn)錄、轉(zhuǎn)錄后和翻譯活動(dòng)的調(diào)節(jié)等仍不清楚。非遺傳多型性如何在不同層次的生物組織中演化及其結(jié)果如何等仍需要進(jìn)一步研究。促進(jìn)非遺傳多型性特性從單一表型狀態(tài)進(jìn)化的基因變化類型至今仍未很好的建立起來，可能包括控制發(fā)育活動(dòng)的細(xì)微變化，如閾值、敏感水平和時(shí)間節(jié)奏的調(diào)節(jié)等。有針對(duì)性的比較研究具有和不具有非遺傳多型性的相近物種可能揭示這些問題[5]。雌性翅的非遺傳多型性與雄性翅的遺傳多態(tài)性的翅的表現(xiàn)型極為相似，與非遺傳多型性相關(guān)的表現(xiàn)型和環(huán)境之間的相互作用可能涉及到與控制遺傳多型性相同的基因位點(diǎn)。翅的非遺傳多型性是一個(gè)明顯的適應(yīng)性表型可塑性的例子，雌性翅的非遺傳多型性與雄性翅的遺傳多型性的共表達(dá)為研究環(huán)境與遺傳誘導(dǎo)的可變表型提供了良好的材料，這有助于弄清遺傳因子和環(huán)境因子是如何交替控制同一發(fā)育結(jié)果，以及這種非遺傳多型性與遺傳多型性之間的進(jìn)化轉(zhuǎn)換是如何發(fā)生的[25]。 控制表型多態(tài)性相關(guān)基因的鑒定，可能會(huì)促進(jìn)非遺傳多型性所產(chǎn)生的相似的表型變化機(jī)制的研究。迄今已有多個(gè)與昆蟲翅發(fā)育相關(guān)的基因獲得鑒定[103, 104]。目前對(duì)遺傳和發(fā)育引起的不同表現(xiàn)型的表達(dá)機(jī)制仍知之不多，基因組學(xué)的研究必將為揭示昆蟲翅多型現(xiàn)象的內(nèi)在機(jī)制提供全新的機(jī)遇[25]。

迄今所涉及的翅多型現(xiàn)象研究對(duì)象絕大多數(shù)為植食性昆蟲，而對(duì)控制害蟲的天敵寄生蜂的翅型分化研究鮮見報(bào)道。目前我國在林業(yè)害蟲生物防治中廣泛應(yīng)用的幾種腫腿蜂均具有翅二型現(xiàn)象，雄性基本有翅而雌性大多數(shù)無翅，其中管氏腫腿蜂(Sclerodermusguani)和川硬皮腫腿蜂(S.sichuanensis)均有無翅型和有翅型2種個(gè)體，雌性主要為無翅型，有翅雌性較少見，而雄性則基本為有翅型，無翅雄性極難見到[16- 19]。白蠟吉丁腫腿蜂(S.pupariae)是近年來發(fā)現(xiàn)的一個(gè)腫腿蜂新種[105]，自然條件下寄生白蠟窄吉丁(Agrilusplanipennis)蛹，后來發(fā)現(xiàn)也能寄生該害蟲的幼蟲和危害白蠟樹的咖啡虎天牛(Xylotrechusgrayii)幼蟲[106]。進(jìn)一步的生物學(xué)研究表明，該蜂可成功寄生柑桔窄吉丁(A.auriventris)、蘋小吉丁(A.mali)、花椒窄吉丁A.zanthoxylumi、核桃脊胸紋吉丁Nalandasp.、復(fù)紋狹天牛(Stenhomaluscomplicatus)、光肩星天牛(Anoplophoraglabripennis)、栗山天牛(Massicusraddei)、松褐天牛(Monochamusalternatus)、麻天牛(Thyestillagebleri)等多種吉丁甲和天牛的幼蟲，且后代均能正常完成生長發(fā)育，是一種非常優(yōu)良的蛀干害蟲天敵[20, 107]。白蠟吉丁腫腿蜂以成蟲越冬，自然種群越冬后成蟲所產(chǎn)的第1代后代中雌性有翅率較高，平均可達(dá)56.6%，第2代則降低到14.7%，此后世代中雌性大多為無翅型。雄性個(gè)體比例較低，約占2%—5%，且雄性基本均為有翅型[20]。這幾種腫腿蜂在我國林業(yè)上廣泛用于防治天牛和吉丁蟲等重要蛀干類害蟲，已實(shí)現(xiàn)工廠化人工大量繁育，但由于繁殖出的雌性基本為無翅型個(gè)體，因此釋放后其擴(kuò)散能力受到限制，只能依靠爬行擴(kuò)散，從而影響了生物防治效果，也給生產(chǎn)應(yīng)用上帶來了不便，在人工放蜂時(shí)需將寄生蜂人為釋放到有寄主害蟲的樹干上，以幫助寄生蜂尋找寄主。因此，如果能明確腫腿蜂發(fā)育過程中翅型分化的機(jī)制，通過人為干預(yù)，培養(yǎng)出較高比例的有翅型雌蜂，釋放后有利于種群的自然擴(kuò)散，提高生物防治效果，將在指導(dǎo)人工大量繁殖高品質(zhì)的寄生蜂個(gè)體用于生產(chǎn)防治上具有重要的指導(dǎo)意義和應(yīng)用價(jià)值。

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Mechanisms of phenotypic plasticity for wing morph differentiation in insects

WANG Xiaoyi, YANG Zhongqi*, WEI Ke, TANG Yanlong

KeyLaboratoryofForestProtection,StateForestryAdministration,ResearchInstituteofForestEcology,EnvironmentandProtection,ChineseAcademyofForestry,Beijing100091,China

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.

wing polymorphism; polyphenism; phenotypic plasticity; adaptive evolution

國家自然科學(xué)基金資助項(xiàng)目(31370654)

2013- 10- 30;

2014- 08- 28

10.5846/stxb201310302610

*通訊作者Corresponding author.E-mail: yangzhqi@126.com

王小藝, 楊忠岐, 魏可, 唐艷龍.昆蟲翅型分化的表型可塑性機(jī)制.生態(tài)學(xué)報(bào),2015,35(12):3988- 3999.

Wang X Y, Yang Z Q, Wei K, Tang Y L.Mechanisms of phenotypic plasticity for wing morph differentiation in insects.Acta Ecologica Sinica,2015,35(12):3988- 3999.