Department for Integrative Evolutionary Biology, Max Planck Institute for Biology Tübingen (MPI-B), Tübingen, Germany.
Evol Dev. 2024 Mar;26(2):e12471. doi: 10.1111/ede.12471. Epub 2024 Feb 14.
Disentangling the evolution of the molecular processes and genetic networks that facilitate the emergence of morphological novelties is one of the main objectives in evolutionary developmental biology. Here, we investigated the evolutionary history of a gene regulatory network controlling the development of novel tooth-like feeding structures in diplogastrid nematodes. Focusing on NHR-1 and NHR-40, the two transcription factors that regulate the morphogenesis of these feeding structures in Pristionchus pacificus, we sought to determine whether they have a similar function in Caenorhabditis elegans, an outgroup species to the Diplogastridae which has typical "rhabditid" flaps instead of teeth. Contrary to our initial expectations, we found that they do not have a similar function. While both receptors are co-expressed in the tissues that produce the feeding structures in the two nematodes, genetic inactivation of either receptor had no impact on feeding-structure morphogenesis in C. elegans. Transcriptomic experiments revealed that NHR-1 and NHR-40 have highly species-specific regulatory targets. These results suggest two possible evolutionary scenarios: either the genetic module responsible for feeding-structure morphogenesis in Diplogastridae already existed in the last common ancestor of C. elegans and P. pacificus, and subsequently disintegrated in the former as NHR-1 and NHR-40 acquired new targets, or it evolved in conjunction with teeth in Diplogastridae. These findings indicate that feeding-structure morphogenesis is regulated by different genetic programs in P. pacificus and C. elegans, hinting at developmental systems drift during the flap-to-tooth transformation. Further research in other "rhabditid" species is needed to fully reconstruct the developmental genetic changes which facilitated the evolution of novel feeding structures in Diplogastridae.
解析分子过程和遗传网络的演化，以促进形态新颖性的出现，是进化发育生物学的主要目标之一。在这里，我们研究了控制双胃线虫新型齿状取食结构发育的基因调控网络的进化历史。我们专注于 NHR-1 和 NHR-40 这两个转录因子，它们调节 Pristionchus pacificus 中这些取食结构的形态发生，试图确定它们在作为 Diplogastridae 外群的 Caenorhabditis elegans 中是否具有类似的功能，而 Diplogastridae 具有典型的“rhabditid”瓣而非牙齿。与我们最初的预期相反，我们发现它们没有类似的功能。虽然这两种受体在两种线虫产生取食结构的组织中共同表达，但受体的遗传失活对 C. elegans 的取食结构形态发生没有影响。转录组实验表明，NHR-1 和 NHR-40 具有高度物种特异性的调控靶标。这些结果提出了两种可能的进化情景：负责 Diplogastridae 取食结构形态发生的遗传模块要么已经存在于 C. elegans 和 P. pacificus 的最后共同祖先中，随后在前者中解体，因为 NHR-1 和 NHR-40 获得了新的靶标，要么与 Diplogastridae 中的牙齿一起进化。这些发现表明，取食结构形态发生在 P. pacificus 和 C. elegans 中受不同的遗传程序调控，这暗示了在瓣到齿的转化过程中发育系统的漂移。需要对其他“rhabditid”物种进行进一步研究，以全面重建促进 Diplogastridae 新型取食结构进化的发育遗传变化。
