Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution.
Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution.
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DOI：
10.1371/journal.pgen.1007375
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发表时间：
2018-05
期刊：
影响因子：
4.5
通讯作者：
McGregor AP
中科院分区：
文献类型：
--
作者：
Kittelmann S;Buffry AD;Franke FA;Almudi I;Yoth M;Sabaris G;Couso JP;Nunes MDS;Frankel N;Gómez-Skarmeta JL;Pueyo-Marques J;Arif S;McGregor AP
趋同表型进化通常是由潜在基因调控网络（GRNs）中特定节点的周期性变化引起的。在这样的进化“热点”的基因被认为是最大限度地影响表型与最小的多效性的后果。这导致了这样的建议，即如果GRN被足够详细地理解，则演化的路径可能是可预测的。果蝇幼虫毛状体的反复进化丧失是由shavenbaby（svb）表达的丧失引起的。svb也是腿部毛状体发育所必需的，但黑腹果蝇T2股骨上“裸谷”中毛状体的进化增益是由microRNA-92 a（miR-92 a）表达减少而不是svb的变化引起的。我们比较了幼虫和腿毛状体GRNs之间的组件的表达和功能，以调查为什么毛状体模式进化的遗传基础在这些发展背景下不同。我们发现这两个网络在所使用的基因以及共同基因的调控和功能方面存在关键差异。GRNs中的这些差异揭示了为什么svb中的突变不太可能有助于腿部毛状体的进化，以及miR-92 a如何在这种情况下代表关键的进化开关。我们的工作表明，在不同的发展背景下，GRN的变异性，以及是否形态特征是失去与获得，影响节点GRN演变，造成形态变化。因此，我们的发现对于理解进化的途径和可预测性具有重要意义。生物学的一个主要目标是确定生物多样性的遗传原因。性状的趋同进化通常是由同一基因的变化引起的，这些基因是进化的“热点”。shavenbaby是果蝇幼虫毛状体损失的“热点”，但microRNA-92 a是腿毛状体增加的基础。为了理解表型进化遗传学中的这种差异，我们比较了潜在调控网络中基因的表达和功能。我们发现，进化的途径受到不同发育背景下基因调控网络结构差异的影响，以及一个性状是丢失还是获得。因此，在一个环境中的热点可能不容易在不同的环境中演变。这对理解表型变化的遗传基础和进化的可预测性具有重要意义。
Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ‘hotspots’ are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ‘naked valley’ on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution. A major goal of biology is to identify the genetic causes of organismal diversity. Convergent evolution of traits is often caused by changes in the same genes–evolutionary ‘hotspots’. shavenbaby is a ‘hotspot’ for larval trichome loss in Drosophila, but microRNA-92a underlies the gain of leg trichomes. To understand this difference in the genetics of phenotypic evolution, we compared the expression and function of genes in the underlying regulatory networks. We found that the pathway of evolution is influenced by differences in gene regulatory network architecture in different developmental contexts, as well as by whether a trait is lost or gained. Therefore, hotspots in one context may not readily evolve in a different context. This has important implications for understanding the genetic basis of phenotypic change and the predictability of evolution.
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