黑森瘿蚊生物型的适合度代价及小麦苗龄对其适合度的影响
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摘要
黑森瘿蚊Mayetiola destructor (Say)是广泛分布于世界主要小麦产区的一种重要小麦害虫。虽然利用抗性品种是控制其危害的最为经济有效的措施，但广泛使用抗虫品种对黑森瘿蚊种群形成的选择压力，导致适应抗性的生物型不断出现，严重制约了抗虫品种的持效期。小麦-黑森瘿蚊系统符合基因对基因（gene-for-gene）模式，为研究昆虫与植物的关系提供了重要依据。害虫在克服寄主抗性的过程中所伴随的适合度代价会影响生物型的进化方向与进程，但在黑森瘿蚊中尚未得到验证。持续筛选抗性材料，分析已知抗虫基因对新生物型的有效性，不仅可以为小麦的抗虫育种提供有用的信息，也可为改进抗虫管理对策提供重要的依据；而探索小麦发育期对黑森瘿蚊适合度的影响则可促进对田间种群动态规律的了解。因此，在实验室条件下，我们研究了黑森瘿蚊生物型分化过程伴随的适合度变化，比较了黑森瘿蚊在不同龄期幼苗上的适合度，评估了栽培二粒小麦的抗虫性，并分析了H13基因适应系（vH13）对已知小麦抗性基因的反应。主要取得如下结果：
1.对两种抗性基因适应型种群H13和H9适应系与非适应生物型Great Plains (GP)的适合度比较结果表明，在去除抗性选择压力的环境下，两个进化种群的成虫个体均小于非适应型，表明黑森瘿蚊对寄主抗性的克服是以降低生殖力为代价的。进一步分析发现，以体型变化来衡量适合度代价的大小，会低估生殖力的损失率。与GP相比，H9适应系与H13适应系雌虫的翅长分别减少了9%和3%，雄虫翅长分别减少了5%和3%；而根据成虫体型大小与繁殖力的关系估计的雌虫产卵量分别减少了32%和12%，雄虫可授精卵量分别减少了18%和11%。
2.比较了抗性基因适应型种群vH13系在两种小麦品种Molly和Newton上的适合度。Molly携带H13基因（新寄主），但最近对vH13系已丧失抗性，Newton不携带任何已知的黑森瘿蚊抗性基因（原始寄主）。结果表明，vH13在两种小麦上的体型大小和发育速率均无明显差别，但在新寄主上，幼虫取食期的存活率，以及卵—成虫期的存活率均显著降低，表明vH13系在选择压力下克服寄主抗性是以降低存活率为代价的。
3.根据苗期对幼虫侵害的反应，从300份栽培二粒小麦品系中筛选出10个抗黑森瘿蚊材料，分别为CItr14972, CItr4013, PI154582, PI94634, PI94650, PI254194, PI362500,PI362501, PI355479和PI377655。其中CItr14972, CItr4013, PI154582, PI362500和PI377655等5种对vH13系表现为高抗。对vH13系的致害力分析表明，在供试的27种抗虫基因（或基因聚合体）中，有5种基因H3, h4, H13, H18和H31已丧失了抗性，而有17种表现高抗，包括H5, H7H8, H9, H11, H12, H14, H15, H17, H19, H20, H21, H22,H25, H26, H28, H29和H32，其中H9, H11, H15, H19, H20, H21, H25, H28和H29等9个基因可作为备选基因用于未来的vH13系流行区。
4.小麦苗龄对黑森瘿蚊的适合度会产生显著影响。分别在2叶期开始取食和5–7叶期开始取食导致在成虫体型大小、卵–成虫的存活率和发育历期均出现显著差异。在小龄植株上的存活率高于大龄幼苗上的个体，发育历期也明显较短，但体型较小。在两种幼苗上卵—成虫的发育历期与成虫的体型之间不存在明显的相关性，获得较大的体型并不必然要求较长的发育时间。对成虫的羽化动态比较发现，大龄幼苗上的雌虫和雄虫均出现两个羽化高峰期，而在小龄麦苗上均只出现一个羽化高峰期。导致大龄幼苗上个体平均发育期较长的原因是羽化期延迟的个体在种群中的比例更高，而非为了获取较大体型所致。
以上结果证实，黑森瘿蚊生物型在克服寄主抗性的致害性进化过程存在适合度代价，在去除抗性选择压力条件下，适合度代价表现为生殖力降低；在有选择压力条件下，表现为存活率降低；小麦的发育期会影响其适合度；栽培二粒小麦也是重要的抗性资源，大部分抗性基因对vH13系是有效的，可用于抗性育种。这些结果为进一步了解黑森瘿蚊生物型的进化过程、种群的田间动态变化规律以及揭示黑森瘿蚊—小麦的协同进化机制提供了重要的理论依据，在实践上可为抗性品种的培育、抗性基因的有效利用和害虫治理提供理论指导。
The Hessian fly, Mayetiola destructor (Say)(Diptera: Cecidomyiidae), is an importantpest of wheat Triticum spp (Poaceae）throughout most of wheat production areas. Resistantwheat varieties have been proved the most reliable and economical form of management forHessian fly. However, the continued development of virulent biotypes in response to selectionpressure imposed by wide-spread use of resistant cultivars poses great threat to thepermanence of resistance. The wheat-Hessian fly system serves as an excellent model forunderstanding plant-insect interactions, especially those involving gene-for-gene interactions.Fitness cost is believed to influence virulence evolution in insect to resistance genes. However,it has not been investigated for the Hessian fly. Screening resistance materials in wheat andanalyzing virulence of impeding virulent genotypes in Hessian fly will provide usefulinformation for wheat breeding program and for improving control strategies for the insect.Investigating interactions between plant ages and insect fitness will facilitate understandingthe dynamics of population in fields. We investigated the fitness changes under laboratoryconditions to1）test the hypothesis that adaptation to resistance couple with fitness cost inHessian fly;2）understand the effect of plant ages on fitness of Hessian fly;3）screenresistance sources in emmer wheat, and4) identify effectiveness of known H genes for a newadapted strain vH13. The main results are as follows:
1. On H-gene-free wheat, two H-adapted strains were shorter to the nonadapted strain inegg-to-adult survival, but they differed in producing adults with shorter wings. By usingknown relationships between wing length and reproductive potential, we found that losses inwing length underestimate reduction in reproductive potential. For example, H9-andH13-adapted females had9%and3%wing reduction, respectively, but they were estimated tohave32%and12%reduction in egg production; for H9-and H13-adapted males, reduction inwing length were5%and3%, respectively, but they were estimated to have18%and11%reduction in reproductive potential.
2. On two wheat lines, one conferring H13resistance (referring to as noval host plant）,another one lacking any known gene (natal host plant), H13-adapted (vH13) populationsshowed no difference in growth rate and adult body size between the two hosts, but they differed in survival. Growing on noval host plant significantly decreased larval survivalduring feeding stage, and reflected on survival from egg-to-adult, indicating that adaptation toH resistance incur reduced survival on noval host, and adaptation to noval host do not resultin decreased performance on natal host.
3. Ten of300accessions of emmer wheat, including CItr14972, CItr4013, PI154582,PI94634, PI94650, PI254194, PI362500, PI362501, PI355479, and PI377655, exhibitedantibiosis resistance to Hessian fly biotype Great Plains. Five of the10lines, includingCItr14972, CItr4013, PI154582, PI362500, and PI377655, exhibited highly resistance to vH13strain. Virulence analysis showed that seventeen of the tested27resisitance genes, H5, H7H8,H9, H11, H12, H14, H15, H17, H19, H20, H21, H22, H25, H26, H28, H29and H32,conferred high levels of resistance (>80%plants resistant）to vH13strain. Five genes, H3, h4,H13, H18, and H31were susceptible (<50%resistant plants). Nine H genes, including H9,H11, H15, H19, H20, H21, H25, H28, and H29should be recommended as candidate genes inareas where vH13strain would be predominant.
4. Plant ages have pleiotropic effects on fitness of the Hessian fly. The insect displayedbetter performance on young seedlings with higher survival from egg to adult and shorteneddevelopment times, with one exception that both females and males were significantly smallerthan those on old seedlings. There was no trade-off between body size and development times.In addition, plant ages lead to a divergence of adult emergence strategy. Relative to adultemergence on young seedlings with one peak, both females and males showed a differentemergence manner with two peaks on old seedlings.
1.对两种抗性基因适应型种群H13和H9适应系与非适应生物型Great Plains (GP)的适合度比较结果表明，在去除抗性选择压力的环境下，两个进化种群的成虫个体均小于非适应型，表明黑森瘿蚊对寄主抗性的克服是以降低生殖力为代价的。进一步分析发现，以体型变化来衡量适合度代价的大小，会低估生殖力的损失率。与GP相比，H9适应系与H13适应系雌虫的翅长分别减少了9%和3%，雄虫翅长分别减少了5%和3%；而根据成虫体型大小与繁殖力的关系估计的雌虫产卵量分别减少了32%和12%，雄虫可授精卵量分别减少了18%和11%。
2.比较了抗性基因适应型种群vH13系在两种小麦品种Molly和Newton上的适合度。Molly携带H13基因（新寄主），但最近对vH13系已丧失抗性，Newton不携带任何已知的黑森瘿蚊抗性基因（原始寄主）。结果表明，vH13在两种小麦上的体型大小和发育速率均无明显差别，但在新寄主上，幼虫取食期的存活率，以及卵—成虫期的存活率均显著降低，表明vH13系在选择压力下克服寄主抗性是以降低存活率为代价的。
3.根据苗期对幼虫侵害的反应，从300份栽培二粒小麦品系中筛选出10个抗黑森瘿蚊材料，分别为CItr14972, CItr4013, PI154582, PI94634, PI94650, PI254194, PI362500,PI362501, PI355479和PI377655。其中CItr14972, CItr4013, PI154582, PI362500和PI377655等5种对vH13系表现为高抗。对vH13系的致害力分析表明，在供试的27种抗虫基因（或基因聚合体）中，有5种基因H3, h4, H13, H18和H31已丧失了抗性，而有17种表现高抗，包括H5, H7H8, H9, H11, H12, H14, H15, H17, H19, H20, H21, H22,H25, H26, H28, H29和H32，其中H9, H11, H15, H19, H20, H21, H25, H28和H29等9个基因可作为备选基因用于未来的vH13系流行区。
4.小麦苗龄对黑森瘿蚊的适合度会产生显著影响。分别在2叶期开始取食和5–7叶期开始取食导致在成虫体型大小、卵–成虫的存活率和发育历期均出现显著差异。在小龄植株上的存活率高于大龄幼苗上的个体，发育历期也明显较短，但体型较小。在两种幼苗上卵—成虫的发育历期与成虫的体型之间不存在明显的相关性，获得较大的体型并不必然要求较长的发育时间。对成虫的羽化动态比较发现，大龄幼苗上的雌虫和雄虫均出现两个羽化高峰期，而在小龄麦苗上均只出现一个羽化高峰期。导致大龄幼苗上个体平均发育期较长的原因是羽化期延迟的个体在种群中的比例更高，而非为了获取较大体型所致。
以上结果证实，黑森瘿蚊生物型在克服寄主抗性的致害性进化过程存在适合度代价，在去除抗性选择压力条件下，适合度代价表现为生殖力降低；在有选择压力条件下，表现为存活率降低；小麦的发育期会影响其适合度；栽培二粒小麦也是重要的抗性资源，大部分抗性基因对vH13系是有效的，可用于抗性育种。这些结果为进一步了解黑森瘿蚊生物型的进化过程、种群的田间动态变化规律以及揭示黑森瘿蚊—小麦的协同进化机制提供了重要的理论依据，在实践上可为抗性品种的培育、抗性基因的有效利用和害虫治理提供理论指导。
The Hessian fly, Mayetiola destructor (Say)(Diptera: Cecidomyiidae), is an importantpest of wheat Triticum spp (Poaceae）throughout most of wheat production areas. Resistantwheat varieties have been proved the most reliable and economical form of management forHessian fly. However, the continued development of virulent biotypes in response to selectionpressure imposed by wide-spread use of resistant cultivars poses great threat to thepermanence of resistance. The wheat-Hessian fly system serves as an excellent model forunderstanding plant-insect interactions, especially those involving gene-for-gene interactions.Fitness cost is believed to influence virulence evolution in insect to resistance genes. However,it has not been investigated for the Hessian fly. Screening resistance materials in wheat andanalyzing virulence of impeding virulent genotypes in Hessian fly will provide usefulinformation for wheat breeding program and for improving control strategies for the insect.Investigating interactions between plant ages and insect fitness will facilitate understandingthe dynamics of population in fields. We investigated the fitness changes under laboratoryconditions to1）test the hypothesis that adaptation to resistance couple with fitness cost inHessian fly;2）understand the effect of plant ages on fitness of Hessian fly;3）screenresistance sources in emmer wheat, and4) identify effectiveness of known H genes for a newadapted strain vH13. The main results are as follows:
1. On H-gene-free wheat, two H-adapted strains were shorter to the nonadapted strain inegg-to-adult survival, but they differed in producing adults with shorter wings. By usingknown relationships between wing length and reproductive potential, we found that losses inwing length underestimate reduction in reproductive potential. For example, H9-andH13-adapted females had9%and3%wing reduction, respectively, but they were estimated tohave32%and12%reduction in egg production; for H9-and H13-adapted males, reduction inwing length were5%and3%, respectively, but they were estimated to have18%and11%reduction in reproductive potential.
2. On two wheat lines, one conferring H13resistance (referring to as noval host plant）,another one lacking any known gene (natal host plant), H13-adapted (vH13) populationsshowed no difference in growth rate and adult body size between the two hosts, but they differed in survival. Growing on noval host plant significantly decreased larval survivalduring feeding stage, and reflected on survival from egg-to-adult, indicating that adaptation toH resistance incur reduced survival on noval host, and adaptation to noval host do not resultin decreased performance on natal host.
3. Ten of300accessions of emmer wheat, including CItr14972, CItr4013, PI154582,PI94634, PI94650, PI254194, PI362500, PI362501, PI355479, and PI377655, exhibitedantibiosis resistance to Hessian fly biotype Great Plains. Five of the10lines, includingCItr14972, CItr4013, PI154582, PI362500, and PI377655, exhibited highly resistance to vH13strain. Virulence analysis showed that seventeen of the tested27resisitance genes, H5, H7H8,H9, H11, H12, H14, H15, H17, H19, H20, H21, H22, H25, H26, H28, H29and H32,conferred high levels of resistance (>80%plants resistant）to vH13strain. Five genes, H3, h4,H13, H18, and H31were susceptible (<50%resistant plants). Nine H genes, including H9,H11, H15, H19, H20, H21, H25, H28, and H29should be recommended as candidate genes inareas where vH13strain would be predominant.
4. Plant ages have pleiotropic effects on fitness of the Hessian fly. The insect displayedbetter performance on young seedlings with higher survival from egg to adult and shorteneddevelopment times, with one exception that both females and males were significantly smallerthan those on old seedlings. There was no trade-off between body size and development times.In addition, plant ages lead to a divergence of adult emergence strategy. Relative to adultemergence on young seedlings with one peak, both females and males showed a differentemergence manner with two peaks on old seedlings.
引文
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