Department of Evolution and Ecology, University of California - Davis, Davis, CA 95616, USA.
Evol Dev. 2011 Nov-Dec;13(6):504-22. doi: 10.1111/j.1525-142X.2011.00507.x.
The diversity of animal and plant forms is shaped by nested evolutionary innovations. Understanding the genetic and molecular changes responsible for these innovations is therefore one of the key goals of evolutionary biology. From the genetic point of view, the origin of novel traits implies the origin of new regulatory pathways to control their development. To understand how these new pathways are assembled in the course of evolution, we need model systems that combine relatively recent innovations with a powerful set of genetic and molecular tools. One such model is provided by the Drosophila sex comb-a male-specific morphological structure that evolved in a relatively small lineage related to the model species D. melanogaster. Our extensive knowledge of sex comb development in D. melanogaster provides the basis for investigating the genetic changes responsible for sex comb origin and diversification. At the same time, sex combs can change on microevolutionary timescales and differ spectacularly among closely related species, providing opportunities for direct genetic analysis and for integrating developmental and population-genetic approaches. Sex comb evolution is associated with the origin of novel interactions between Hox and sex determination genes. Activity of the sex determination pathway was brought under the control of the Hox code to become segment-specific, while Hox gene expression became sexually dimorphic. At the same time, both Hox and sex determination genes were integrated into the intrasegmental spatial patterning network, and acquired new joint downstream targets. Phylogenetic analysis shows that similar sex comb morphologies evolved independently in different lineages. Convergent evolution at the phenotypic level reflects convergent changes in the expression of Hox and sex determination genes, involving both independent gains and losses of regulatory interactions. However, the downstream cell-differentiation programs have diverged between species, and in some lineages, similar adult morphologies are produced by different morphogenetic mechanisms. These features make the sex comb an excellent model for examining not only the genetic changes responsible for its evolution, but also the cellular processes that translate DNA sequence changes into morphological diversity. The origin and diversification of sex combs provides insights into the roles of modularity, cooption, and regulatory changes in evolutionary innovations, and can serve as a model for understanding the origin of the more drastic novelties that define higher order taxa.
动物和植物形态的多样性是由嵌套的进化创新形成的。因此，理解导致这些创新的遗传和分子变化是进化生物学的关键目标之一。从遗传的角度来看，新特征的起源意味着需要控制其发育的新调控途径的起源。为了了解这些新途径在进化过程中是如何组装的，我们需要结合相对较新的创新和一套强大的遗传和分子工具的模型系统。果蝇的性梳就是这样一个模型，它是在与模型物种黑腹果蝇相关的一个相对较小的谱系中进化而来的一种雄性特有的形态结构。我们对黑腹果蝇性梳发育的广泛了解为研究导致性梳起源和多样化的遗传变化提供了基础。同时，性梳可以在微观进化时间尺度上发生变化，并在密切相关的物种之间差异显著，这为直接的遗传分析以及整合发育和群体遗传学方法提供了机会。性梳的进化与 Hox 和性别决定基因之间新的相互作用的起源有关。性别决定途径的活性受 Hox 密码的控制，变得具有节段特异性，而 Hox 基因表达变得性别二态。同时，Hox 和性别决定基因都被整合到节段内的空间模式网络中，并获得了新的共同下游靶标。系统发育分析表明，不同谱系中独立进化出了相似的性梳形态。表型水平的趋同进化反映了 Hox 和性别决定基因表达的趋同变化，涉及到调控相互作用的独立获得和丧失。然而，物种之间的下游细胞分化程序已经分化，在一些谱系中，相似的成虫形态是由不同的形态发生机制产生的。这些特征使得性梳成为一个极好的模型，不仅可以研究导致其进化的遗传变化，还可以研究将 DNA 序列变化转化为形态多样性的细胞过程。性梳的起源和多样化为研究模块性、共适应和进化创新中的调控变化的作用提供了启示，并可以作为理解定义更高分类群的更剧烈新奇性起源的模型。
