Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.
J Evol Biol. 2024 Jul 10;37(7):758-769. doi: 10.1093/jeb/voae047.
Domains as functional protein units and their rearrangements along the phylogeny can shed light on the functional changes of proteomes associated with the evolution of complex traits like eusociality. This complex trait is associated with sterile soldiers and workers, and long-lived, highly fecund reproductives. Unlike in Hymenoptera (ants, bees, and wasps), the evolution of eusociality within Blattodea, where termites evolved from within cockroaches, was accompanied by a reduction in proteome size, raising the question of whether functional novelty was achieved with existing rather than novel proteins. To address this, we investigated the role of domain rearrangements during the evolution of termite eusociality. Analysing domain rearrangements in the proteomes of three solitary cockroaches and five eusocial termites, we inferred more than 5,000 rearrangements over the phylogeny of Blattodea. The 90 novel domain arrangements that emerged at the origin of termites were enriched for several functions related to longevity, such as protein homeostasis, DNA repair, mitochondrial activity, and nutrient sensing. Many domain rearrangements were related to changes in developmental pathways, important for the emergence of novel castes. Along with the elaboration of social complexity, including permanently sterile workers and larger, foraging colonies, we found 110 further domain arrangements with functions related to protein glycosylation and ion transport. We found an enrichment of caste-biased expression and splicing within rearranged genes, highlighting their importance for the evolution of castes. Furthermore, we found increased levels of DNA methylation among rearranged compared to non-rearranged genes suggesting fundamental differences in their regulation. Our findings indicate the importance of domain rearrangements in the generation of functional novelty necessary for termite eusociality to evolve.
结构域作为功能蛋白单元，其在系统发育过程中的重排可以揭示与社会性等复杂特征进化相关的蛋白质组的功能变化。这种复杂特征与不育的兵蚁和工蚁以及寿命长、繁殖力强的生殖蚁有关。与膜翅目（蚂蚁、蜜蜂和胡蜂）不同，在蜚蠊目（蟑螂）中社会性的进化伴随着蛋白质组大小的减少，这就提出了一个问题，即功能的新颖性是否是通过现有的而不是新的蛋白质来实现的。为了解决这个问题，我们研究了在白蚁社会性进化过程中结构域重排的作用。通过分析三种独居蟑螂和五种社会性白蚁的蛋白质组中的结构域重排，我们推断在蜚蠊目系统发育过程中发生了超过 5000 次重排。在白蚁起源时出现的 90 种新的结构域排列富集了几个与长寿相关的功能，如蛋白质稳态、DNA 修复、线粒体活性和营养感应。许多结构域重排与发育途径的变化有关，这些变化对新的形态发生很重要。随着社会复杂性的发展，包括永久性不育的工蚁和更大的觅食群体，我们还发现了 110 个与蛋白质糖基化和离子转运相关的功能的进一步结构域排列。我们发现，在重排基因中存在着与形态相关的表达和剪接的富集，这突出了它们对形态进化的重要性。此外，我们发现与非重排基因相比，重排基因中的 DNA 甲基化水平升高，这表明它们在调控方面存在根本差异。我们的研究结果表明，结构域重排在产生白蚁社会性所必需的功能新颖性方面具有重要意义。
