Vitellogenin underwent subfunctionalization to acquire caste and behavioral specific expression in the harvester ant Pogonomyrmex barbatus.
Vitellogenin underwent subfunctionalization to acquire caste and behavioral specific expression in the harvester ant Pogonomyrmex barbatus.
复制标题
DOI：
10.1371/journal.pgen.1003730
复制
发表时间：
2013
期刊：
影响因子：
4.5
通讯作者：
Keller L
中科院分区：
文献类型：
--
作者：
Corona M;Libbrecht R;Wurm Y;Riba-Grognuz O;Studer RA;Keller L
生殖平面假说（RGPH）提出，调节生殖的生理途径被用来调节工人的劳动分工。研究证明，工蜂的繁殖潜力（通过卵黄蛋白原 (Vg) 水平评估）与任务表现相关，为蜜蜂的这一假设提供了支持。有趣的是，与具有单一 Vg 直系同源物和潜在可生育的护士的蜜蜂相反，收获蚁 Pogonomyrmex barbatus 的基因组含有两个 Vg 基因（Pb_Vg1 和 Pb_Vg2），并且护士产生不育的营养卵。因此，P. barbatus 提供了一个独特的模型来研究蚂蚁中 Vg 复制是否随后进行亚功能化以获得生殖和非生殖功能，以及 Vg 生殖功能是否被增选来调节不育工蚁的行为。为了研究这些问题，我们比较了P. barbatus Vg基因的表达模式，并分析了蚂蚁中Vg基因的系统发育关系和分子进化。 qRT-PCR 显示，与工蜂相比，Pb_Vg1 在蜂王中表达更高，与觅食者相比，在护士中表达更高。相比之下，觅食者中 Pb_Vg2 的表达水平高于护士和蚁后。系统发育分析表明，祖先 Vg 基因的第一次重复发生在类火蚁和蚁类分支之间的分歧之后，随后的重复发生在导致红火蚁、Linepithema humile 和 Acromyrmex echinatior 的谱系中。最初的重复导致两个 Vg 基因亚家族优先在蚁后和护士（亚科 A）或觅食工蚁（亚科 B）中表达。最后，分子进化分析表明，A亚科经历了正选择，而B亚科则表现出总体松弛的纯化选择。我们的结果表明，在 P. barbatus 中，Vg 基因在复制后经历了亚功能化，以获得与生殖和非生殖功能相关的种姓和行为特异性表达，支持了 RGPH 在蚂蚁中的有效性。社会性昆虫的主要特征之一是劳动分工，蚁后垄断繁殖，而不育工蜂则执行与群体维护相关的所有任务。工蚁这样做的顺序通常与年龄有关：年轻的工蚁倾向于在巢内照顾幼崽，年长的工蚁更有可能寻找食物。先前的研究表明，卵黄蛋白原（一种通常参与调节独居昆虫繁殖的卵黄蛋白）已被用来调节蜜蜂的劳动分工。在这项研究中，我们研究了卵黄蛋白原在另一群群居昆虫：蚂蚁中的作用。我们首先使用系统发育分析来揭示大多数已测序的蚂蚁基因组中存在多个卵黄蛋白原基因。然后我们比较了种子收获蚁 Pogonomyrmex barbatus 的蚁后、护士和觅食者中两个卵黄蛋白原基因（Pb_Vg1 和 Pb_Vg2）的表达。我们的结果表明，在蚂蚁中最初复制后，卵黄蛋白原基因获得了与生殖和非生殖营养相关功能相关的种姓和行为特异性表达。这项研究还表明，蚂蚁和蜜蜂尽管独立进化出了社会性，但仍保留了类似的调节劳动分工的机制。
The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1 and Pb_Vg2) and nurses produce infertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of P. barbatus Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that Pb_Vg1 is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of Pb_Vg2 was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to Solenopsis invicta, Linepithema humile and Acromyrmex echinatior. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in P. barbatus the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants. One of the main features of social insects is the division of labor, whereby queens monopolize reproduction while sterile workers perform all of the tasks related to colony maintenance. The workers usually do so in an age-dependent sequence: young workers tend to nurse the brood inside the nest and older workers are more likely to forage for food. Previous studies revealed that vitellogenin, a yolk protein typically involved in the regulation of reproduction in solitary insects, has been co-opted to regulate division of labor in the honeybee. In this study, we investigate such a role of vitellogenin in another group of social insects: the ants. We first use phylogenetic analyses to reveal the existence of multiple vitellogenin genes in most of the sequenced ant genomes. Then we compare the expression of the two vitellogenin genes (Pb_Vg1 and Pb_Vg2) among queens, nurses and foragers in the seed-harvester ant Pogonomyrmex barbatus. Our results suggest that, after the initial duplication in ants, the vitellogenin genes acquired caste and behavioral specific expression associated with reproductive and non-reproductive nutritionally related functions. This study also shows that ants and bees, despite having evolved sociality independently, have conserved similar mechanisms to regulate division of labor.
登录
查看更多内容
影响因子：
56.9
作者：
Ben-Shahar, Y;Robichon, A;Robinson, GE
通讯作者：
Robinson, GE
影响因子：
2.2
作者：
Cremonez, TM;De Jong, D;Bitondi, MMG
通讯作者：
Bitondi, MMG
影响因子：
64.8
作者：
Amdam, GV;Csondes, A;Page, RE
通讯作者：
Page, RE
影响因子：
2.2
作者：
Dolezal, Adam G.;Johnson, Joshua;Amdam, Gro V.
通讯作者：
Amdam, Gro V.
DOI：
10.1093/bioinformatics/btp348
发表时间：
2009-08-01
期刊：
Bioinformatics (Oxford, England)
影响因子：
--
作者：
Capella-Gutiérrez S;Silla-Martínez JM;Gabaldón T
通讯作者：
Gabaldón T