Gross Joshua B, Berning Daniel, Phelps Ayana, Luc Heidi
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, United States.
Front Cell Dev Biol. 2023 Feb 15;11:1074616. doi: 10.3389/fcell.2023.1074616. eCollection 2023.
The biological basis of lateralized cranial aberrations can be rooted in early asymmetric patterning of developmental tissues. However, precisely how development impacts natural cranial asymmetries remains incompletely understood. Here, we examined embryonic patterning of the cranial neural crest at two phases of embryonic development in a natural animal system with two morphotypes: cave-dwelling and surface-dwelling fish. Surface fish are highly symmetric with respect to cranial form at adulthood, however adult cavefish harbor diverse cranial asymmetries. To examine if lateralized aberrations of the developing neural crest underpin these asymmetries, we used an automated technique to quantify the area and expression level of cranial neural crest markers on the left and right sides of the embryonic head. We examined the expression of marker genes encoding both structural proteins and transcription factors at two key stages of development: 36 hpf (∼mid-migration of the neural crest) and 72 hpf (∼early differentiation of neural crest derivatives). Interestingly, our results revealed asymmetric biases at both phases of development in both morphotypes, however consistent lateral biases were less common in surface fish as development progressed. Additionally, this work provides the information on neural crest development, based on whole-mount expression patterns of 19 genes, between stage-matched cave and surface morphs. Further, this study revealed 'asymmetric' noise as a likely normative component of early neural crest development in natural fish. Mature cranial asymmetries in cave morphs may arise from persistence of asymmetric processes during development, or as a function of asymmetric processes occurring later in the life history.
颅骨侧化畸变的生物学基础可能源于发育组织早期的不对称模式形成。然而,发育如何精确影响自然颅骨不对称性仍未完全清楚。在此,我们在一个具有两种形态类型的自然动物系统中,研究了胚胎发育两个阶段的颅神经嵴的胚胎模式形成,这两种形态类型为:穴居鱼和表层鱼。成年表层鱼的颅骨形态高度对称,然而成年穴居鱼存在多种颅骨不对称情况。为了研究发育中的神经嵴的侧化畸变是否是这些不对称性的基础,我们使用一种自动化技术来量化胚胎头部左右两侧颅神经嵴标志物的面积和表达水平。我们在发育的两个关键阶段检测了编码结构蛋白和转录因子的标志物基因的表达:受精后36小时(神经嵴大约处于迁移中期)和受精后72小时(神经嵴衍生物大约处于早期分化阶段)。有趣的是,我们的结果显示,在两种形态类型的发育两个阶段均存在不对称偏差,然而随着发育的进行,一致的侧向偏差在表层鱼中不太常见。此外,这项工作基于19个基因的整体表达模式,提供了阶段匹配的穴居和表层形态之间神经嵴发育的信息。此外,这项研究揭示“不对称”噪声可能是自然鱼类早期神经嵴发育的一个正常组成部分。穴居形态中成熟的颅骨不对称可能源于发育过程中不对称过程的持续存在,或者是生命史后期发生的不对称过程的一种作用。