BACKGROUND How novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo. The insect head represents an ancient body region patterned by a deeply conserved developmental genetic network, yet at the same time constitutes a hot spot for morphological innovation. However, the mechanisms that facilitate the repeated emergence, integration, and diversification of morphological novelties within this body region are virtually unknown. Using horned Onthophagus beetles, we investigated the mechanisms that instruct the development of the dorsal adult head and the formation and integration of head horns, one of the most elaborate classes of secondary sexual weapons in the animal kingdom. RESULTS Using region-specific RNAseq and gene knockdowns, we (i) show that the head is compartmentalized along multiple axes, (ii) identify striking parallels between morphological and transcriptional complexity across regions, yet (iii) fail to identify a horn-forming gene module. Instead, (iv) our results support that sex-biased regulation of a shared transcriptional repertoire underpins the formation of horned and hornless heads. Furthermore, (v) we show that embryonic head patterning genes frequently maintain expression within the dorsal head well into late post-embryonic development, thereby possibly facilitating the repurposing of such genes within novel developmental contexts. Lastly, (vi) we identify novel functions for several genes including three embryonic head patterning genes in the integration of both posterior and anterior head horns. CONCLUSIONS Our results illuminate how the adult insect head is patterned and suggest mechanisms capable of integrating novel traits within ancient trait complexes in a sex- and species-specific manner. More generally, our work underscores how significant morphological innovation in developmental evolution need not require the recruitment of new genes, pathways, or gene networks but instead may be scaffolded by pre-existing developmental machinery.

中文翻译：

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将进化上新颖的角整合到高度保守的昆虫头中。

背景技术新特质如何在不损害祖先功能的情况下整合到古代特质复合物中是evo-devo的基本挑战。昆虫的头部代表着一个古老的身体区域，它由一个高度保守的发育遗传网络组成，但同时也构成了形态创新的热点。但是，促进这种身体区域内形态新颖性的反复出现，整合和多样化的机制实际上是未知的。我们使用有角的食虫甲虫，研究了指导成年背头发育以及头角的形成和整合的机制，头角是动物界中最复杂的次级性武器之一。结果使用区域特异性RNAseq和基因敲低，我们（i）显示头部沿多个轴被分隔，（ii）识别出跨区域的形态学和转录复杂性之间惊人的相似之处，但（iii）无法识别出形成角的基因模块。取而代之的是，（iv）我们的研究结果支持对共享转录谱库进行性别偏见调节，从而支持有角和无角头的形成。此外，（v）我们显示，胚胎头模式基因经常在背头内良好地维持表达，直至胚​​胎后发育后期，从而可能促进此类基因在新的发育环境中的重新利用。最后，（vi）我们确定了几个基因的新功能，包括后头角和前头角的整合中的三个胚胎头模式基因。结论我们的研究结果阐明了成虫的昆虫头是如何形成图案的，并提出了能够以性别和物种特异性的方式将古代性状复合体中的新性状整合的机制。更广泛地讲，我们的工作强调了在发育进化中的重大形态创新不需要新基因，途径或基因网络的募集，而是可以由已有的发育机制来支撑。