Female behaviour drives expression and evolution of gustatory receptors in butterflies.

Female behaviour drives expression and evolution of gustatory receptors in butterflies.
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DOI:
10.1371/journal.pgen.1003620
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发表时间:
2013
期刊:
影响因子:
4.5
通讯作者:
Jiggins CD
Jiggins CD
中科院分区:
生物学2区
文献类型:
--
作者:
Briscoe AD;Macias-Muñoz A;Kozak KM;Walters JR;Yuan F;Jamie GA;Martin SH;Dasmahapatra KK;Ferguson LC;Mallet J;Jacquin-Joly E;Jiggins CD

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次生植物化合物是昆虫产卵和取食的强烈阻遏物,但也可能是专门的食草动物的引诱剂。这些昆虫-植物相互作用是由昆虫味觉受体(Grs)和嗅觉受体(Ors)介导的。以西番莲藤为食的蝴蝶Heliconius melpomene的参考基因组分析,与全基因组测序的物种内,并在整个Heliconiusacrogeny允许一个前所未有的机会,研究这些关键的感觉基因之间的基因复制和拷贝数变异(CNV)的模式。我们报告了73个Gr基因在H. melpomene参考基因组,包括推定的CO2,糖,糖醇,果糖和苦味受体。这些Grs中的大多数是基因复制的结果,因为Heliconius与帝王蝶或丝绸有共同的祖先。在Grs而不是Ors中,CNVs在那些在进化时间尺度上也复制的基因谱系中的物种内更常见,这表明正在进行的快速基因家族进化。对来自成年H的长鼻和唇须、触角和腿的转录组进行深度测序(1010亿读取)。黑色素瘤男性和女性的基因组学结果表明,预测的73个Gr基因中的67个和预测的70个Or基因中的67个在这三种组织中表达。有趣的是,我们发现三分之一的所有Grs显示女性偏向的基因表达(n = 26),几乎所有这些(n = 21)是螺旋属特异性Grs。    事实上,在女性腿部而不是男性腿部表达的Grs的显著过量是最近基因复制的结果。两性之间Gr基因表达多样性的这种差异伴随着H前肢上味觉感受器丰度的显著性二型性。melpomene,这表明雌性产卵行为驱动了蝴蝶基因组中新味觉受体的进化。昆虫和它们的化学防御寄主植物参与了一场共同进化的军备竞赛,但昆虫识别合适寄主植物的遗传基础却知之甚少。寄主植物的特化需要昆虫专门的传感器来利用新的生态位。成年的雄性和雌性Heliconius蝴蝶以花蜜为食,而对于蝴蝶来说,不寻常的是,它们以花朵的花粉为食,而它们的幼虫则以西番莲藤的叶子为食。我们已经发现,蝴蝶亚种之间固定的差异,在拷贝数的变化之间的几个假定的糖受体基因,位于不同的染色体,提高当地适应周围的糖检测的可能性。我们还表明,腿的成年雌性蝴蝶,这是由女性选择的寄主植物上产卵时,表达更多的味觉(味道)受体基因比雄性蝴蝶。这些女性偏好的味觉受体显示出显着更高的水平的基因复制比一组味觉受体在两性中表达。因此,性别限制的行为可能会影响生理上重要的基因家族的长期进化,从而产生强烈的生态适应基因组特征。
Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors (Grs) and olfactory receptors (Ors). An analysis of the reference genome of the butterfly Heliconius melpomene, which feeds on passion-flower vines (Passiflora spp.), together with whole-genome sequencing within the species and across the Heliconius phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report in silico gene predictions of 73 Gr genes in the H. melpomene reference genome, including putative CO2, sugar, sugar alcohol, fructose, and bitter receptors. The majority of these Grs are the result of gene duplications since Heliconius shared a common ancestor with the monarch butterfly or the silkmoth. Among Grs but not Ors, CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing (∼1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult H. melpomene males and females indicates that 67 of the predicted 73 Gr genes and 67 of the 70 predicted Or genes are expressed in these three tissues. Intriguingly, we find that one-third of all Grs show female-biased gene expression (n = 26) and nearly all of these (n = 21) are Heliconius-specific Grs. In fact, a significant excess of Grs that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in Gr gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of H. melpomene, suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes. Insects and their chemically-defended hostplants engage in a co-evolutionary arms race but the genetic basis by which suitable host plants are identified by insects is poorly understood. Host plant specializations require specialized sensors by the insects to exploit novel ecological niches. Adult male and female Heliconius butterflies feed on nectar and, unusually for butterflies, on pollen from flowers while their larvae feed on the leaves of passion-flower vines. We have discovered–between sub-species of butterflies-fixed differences in copy-number variation among several putative sugar receptor genes that are located on different chromosomes, raising the possibility of local adaptation around the detection of sugars. We also show that the legs of adult female butterflies, which are used by females when selecting a host plant on which to lay their eggs, express more gustatory (taste) receptor genes than those of male butterflies. These female-biased taste receptors show a significantly higher level of gene duplication than a set of taste receptors expressed in both sexes. Sex-limited behaviour may therefore influence the long-term evolution of physiologically important gene families resulting in a strong genomic signature of ecological adaptation.
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发表时间: 2007-01-01
影响因子: --
作者:
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通讯作者: Gilbert, Lawrence E.
DOI: 10.1038/nature06341
发表时间: 2007-11-08
期刊: NATURE
影响因子: 64.8
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期刊: NATURE
影响因子: 64.8
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Dasmahapatra, Kanchon K.;Walters, James R.;Briscoe, Adriana D.;Davey, John W.;Whibley, Annabel;Nadeau, Nicola J.;Zimin, Aleksey V.;Hughes, Daniel S. T.;Ferguson, Laura C.;Martin, Simon H.;Salazar, Camilo;Lewis, James J.;Adler, Sebastian;Ahn, Seung-Joon;Baker, Dean A.;Baxter, Simon W.;Chamberlain, Nicola L.;Chauhan, Ritika;Counterman, Brian A.;Dalmay, Tamas;Gilbert, Lawrence E.;Gordon, Karl;Heckel, David G.;Hines, Heather M.;Hoff, Katharina J.;Holland, Peter W. H.;Jacquin-Joly, Emmanuelle;Jiggins, Francis M.;Jones, Robert T.;Kapan, Durrell D.;Kersey, Paul;Lamas, Gerardo;Lawson, Daniel;Mapleson, Daniel;Maroja, Luana S.;Martin, Arnaud;Moxon, Simon;Palmer, William J.;Papa, Riccardo;Papanicolaou, Alexie;Pauchet, Yannick;Ray, David A.;Rosser, Neil;Salzberg, Steven L.;Supple, Megan A.;Surridge, Alison;Tenger-Trolander, Ayse;Vogel, Heiko;Wilkinson, Paul A.;Wilson, Derek;Yorke, James A.;Yuan, Furong;Balmuth, Alexi L.;Eland, Cathlene;Gharbi, Karim;Thomson, Marian;Gibbs, Richard A.;Han, Yi;Jayaseelan, Joy C.;Kovar, Christie;Mathew, Tittu;Muzny, Donna M.;Ongeri, Fiona;Pu, Ling-Ling;Qu, Jiaxin;Thornton, Rebecca L.;Worley, Kim C.;Wu, Yuan-Qing;Linares, Mauricio;Blaxter, Mark L.;Ffrench-Constant, Richard H.;Joron, Mathieu;Kronforst, Marcus R.;Mullen, Sean P.;Reed, Robert D.;Scherer, Steven E.;Richards, Stephen;Mallet, James;McMillan, W. Owen;Jiggins, Chris D.
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