Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Germany.
Zoology/Evolutionary Biology, University of Regensburg, Regensburg, Germany.
Mol Ecol. 2022 Oct;31(19):4991-5004. doi: 10.1111/mec.16639. Epub 2022 Aug 17.
The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste exhibits highly specialized morphology, behaviour, and life-history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave-making versus host ants) across five independent origins of ant slavery in the "Formicoxenus-group" of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than in nonparasitic ants, we also compare caste-specific gene expression patterns between lifestyles. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated modules of coexpressed genes with strong connectivity. However, several genes and one gene module are linked to slave-making across the independent origins of this parasitic lifestyle, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences in gene expression remain consistent even when species switch to a parasitic lifestyle. Our findings strongly support the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, as proposed by the "genetic toolkit" hypothesis.
社会性膜翅目昆虫(蚂蚁、蜜蜂、胡蜂)的生态成功依赖于蜂王和工蜂之间的分工。每个蜂群都表现出高度专门化的形态、行为和生活史特征,如寿命和繁殖力。尽管昆虫社会具有强烈的防御外来入侵者的能力,但它们仍然容易受到社会寄生虫的侵害,例如没有工蜂的寄生者或奴役蚂蚁。在这里,我们调查了在 Crematogastrini 蚂蚁部落的“Formicoxenus 组”中,五种独立起源的奴役蚂蚁中,生活方式(奴役蚂蚁与宿主蚂蚁)之间的基因表达是否以类似的方式发生变化。由于在奴役蚂蚁中,与非寄生蚂蚁相比,蜂群之间的差异通常不太明显,因此我们还比较了生活方式之间的特定蜂群基因表达模式。我们证明了,无论生活方式如何,蜂王和工蜂之间的表达差异在不同的分类群中都有很大的重叠。蜂群比生活方式更能深刻地影响转录组,这表明与生活方式相比,有 37 倍以上的基因与蜂群有关,而与生活方式有关的基因则有 37 倍以上,并且与具有强连接性的共表达基因的多个蜂群相关模块有关。然而,有几个基因和一个基因模块与这种寄生生活方式的独立起源有关,这表明存在一些进化趋同。最后,我们没有发现基因表达与生活方式之间存在相互作用的证据,这表明即使物种转变为寄生生活方式,基因表达的蜂群差异仍然保持一致。我们的研究结果强烈支持了一个核心基因集的存在,这些基因的表达与这个蚂蚁类群中的蜂王和工蜂蜂群有关,正如“遗传工具包”假说所提出的那样。