Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, 48109.
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, 20147.
Evolution. 2020 Jun;74(6):1098-1111. doi: 10.1111/evo.13990. Epub 2020 May 17.
The evolution of sexual traits often involves correlated changes in morphology and behavior. For example, in Drosophila, divergent mating displays are often accompanied by divergent pigment patterns. To better understand how such traits co-evolve, we investigated the genetic basis of correlated divergence in wing pigmentation and mating display between the sibling species Drosophila elegans and Drosophila gunungcola. Drosophila elegans males have an area of black pigment on their wings known as a wing spot and appear to display this spot to females by extending their wings laterally during courtship. By contrast, D. gunungcola lost both of these traits. Using Multiplexed Shotgun Genotyping (MSG), we identified a ∼440 kb region on the X chromosome that behaves like a genetic switch controlling the presence or absence of male-specific wing spots. This region includes the candidate gene optomotor-blind (omb), which plays a critical role in patterning the Drosophila wing. The genetic basis of divergent wing display is more complex, with at least two loci on the X chromosome and two loci on autosomes contributing to its evolution. Introgressing the X-linked region affecting wing spot development from D. gunungcola into D. elegans reduced pigmentation in the wing spots but did not affect the wing display, indicating that these are genetically separable traits. Consistent with this observation, broader sampling of wild D. gunungcola populations confirmed that the wing spot and wing display are evolving independently: some D. gunungcola males performed wing displays similar to D. elegans despite lacking wing spots. These data suggest that correlated selection pressures rather than physical linkage or pleiotropy are responsible for the coevolution of these morphological and behavioral traits. They also suggest that the change in morphology evolved prior to the change in behavior.
性特征的进化通常涉及形态和行为的相关变化。例如，在果蝇中，不同的交配展示通常伴随着不同的色素模式。为了更好地理解这些特征是如何共同进化的，我们研究了姐妹种果蝇elegans 和果蝇 gunungcola 之间翅膀色素和交配展示相关分歧的遗传基础。果蝇 elegans 雄蝇翅膀上有一个黑色的斑点，称为翅斑，在求偶时，它们似乎通过侧向伸展翅膀来向雌蝇展示这个斑点。相比之下，D. gunungcola 失去了这两个特征。使用多重散弹枪基因分型 (MSG)，我们在 X 染色体上鉴定出一个约 440 kb 的区域，该区域的行为类似于控制雄性特异性翅斑存在或缺失的遗传开关。这个区域包括候选基因 optomotor-blind (omb)，它在果蝇翅膀的模式形成中起着关键作用。分歧的翅膀展示的遗传基础更为复杂，X 染色体上至少有两个基因座和常染色体上的两个基因座对其进化有贡献。将影响翅斑发育的 X 连锁区域从 D. gunungcola 引入 D. elegans 减少了翅斑的色素沉着，但不影响翅膀展示，表明这些是遗传上可分离的特征。这一观察结果与更广泛的野生 D. gunungcola 种群样本一致，证实了翅斑和翅膀展示正在独立进化：尽管一些 D. gunungcola 雄蝇缺乏翅斑，但它们表现出类似于 D. elegans 的翅膀展示。这些数据表明，相关的选择压力而不是物理连锁或多效性是导致这些形态和行为特征共同进化的原因。它们还表明，形态的变化先于行为的变化而发生。
