Department of Biology, University of Dayton, Dayton, Ohio, USA.
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
J Exp Zool B Mol Dev Evol. 2023 Mar;340(2):143-161. doi: 10.1002/jez.b.23068. Epub 2021 Jul 12.
Changes in gene expression are a prominent feature of morphological evolution. These changes occur to hierarchical gene regulatory networks (GRNs) of transcription factor genes that regulate the expression of trait-building differentiation genes. While changes in the expression of differentiation genes are essential to phenotypic evolution, they can be caused by mutations within cis-regulatory elements (CREs) that drive their expression (cis-evolution) or within genes for CRE-interacting transcription factors (trans-evolution). Locating these mutations remains a challenge, especially when experiments are limited to one species that possesses the ancestral or derived phenotype. We investigated CREs that control the expression of the differentiation genes tan and yellow, the expression of which evolved during the gain, modification, and loss of dimorphic pigmentation among Sophophora fruit flies. We show these CREs to be necessary components of a pigmentation GRN, as deletion from Drosophila melanogaster (derived dimorphic phenotype) resulted in lost expression and lost male-specific pigmentation. We evaluated the ability of orthologous CRE sequences to drive reporter gene expression in species with modified (Drosophila auraria), secondarily lost (Drosophila ananassae), and ancestrally absent (Drosophila willistoni) pigmentation. We show that the transgene host frequently determines CRE activity, implicating trans-evolution as a significant factor for this trait's diversity. We validated the gain of dimorphic Bab transcription factor expression as a trans-change contributing to the dimorphic trait. Our findings suggest an amenability to change for the landscape of trans-regulators and begs for an explanation as to why this is so common compared to the evolution of differentiation gene CREs.
基因表达的变化是形态进化的一个突出特征。这些变化发生在转录因子基因的层次化基因调控网络（GRN）中，这些基因调控着性状形成分化基因的表达。虽然分化基因表达的变化对于表型进化至关重要，但它们也可能是由于驱动其表达的顺式调控元件（CREs）内的突变（顺式进化）或 CRE 相互作用转录因子基因内的突变（反式进化）引起的。定位这些突变仍然是一个挑战，特别是当实验仅限于具有祖先或衍生表型的一个物种时。我们研究了控制分化基因 tan 和 yellow 表达的 CREs，这些基因的表达在 Sophophora 果蝇的二态性色素沉着获得、修饰和丧失过程中发生了进化。我们表明，这些 CREs 是色素沉着 GRN 的必要组成部分，因为从果蝇（衍生的二态表型）中删除这些 CRE 导致表达丧失和雄性特异性色素丧失。我们评估了同源 CRE 序列在具有修饰（果蝇 auraria）、次要丧失（果蝇 ananassae）和祖先缺失（果蝇 willistoni）色素沉着的物种中驱动报告基因表达的能力。我们表明，转基因宿主经常决定 CRE 活性，这表明反式进化是该性状多样性的一个重要因素。我们验证了二态性 Bab 转录因子表达的获得是导致二态性性状的反式变化。我们的研究结果表明，反式调控因子的变化景观具有可变性，并要求解释为什么与分化基因 CREs 的进化相比，这种情况如此普遍。
