Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns

Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns
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DOI:
10.1016/j.cub.2019.10.010
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发表时间:
2019-12-02
期刊:
影响因子:
9.2
通讯作者:
McMillan, W. Owen
McMillan, W. Owen
中科院分区:
生物学1区
文献类型:
--
作者:
Concha, Carolina;Wallbank, Richard W. R.;McMillan, W. Owen

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我们能在多大程度上预测进化是如何发生的?遗传结构和发育过程是否以一种可预测的方式引导类似结果的进化?或者,历史偶然性是否会迫使我们选择另一种途径来应对同样的挑战?近亲蝴蝶之间的穆勒氏模仿提供了进化的自然复制,使我们能够测试相同的翅膀图案是否遵循平行或新的轨迹。在这里,我们探讨了信号配体WntA在蝴蝶中产生模仿翅膀图案的作用,蝴蝶是一个具有非凡模仿相关翅膀图案多样性的群体。辐射是相对年轻的,在过去的2.5-4.5 Ma中已经进化出了许多翅膀模式模仿的案例。WntA是自然选择的一个重要目标,是导致群体模式变异的四个主要效应位点之一。我们使用CRISPR/Cas9靶向诱变技术,在12个物种和另外10个种内变异中产生了wnta缺陷的翅膀,其中包括3个模拟对。在所有被测试的蝴蝶中,WntA敲除广泛地影响模式,并导致每一种可能的鳞片细胞类型的转变。有趣的是,缺乏WntA的基因组非常不同,这表明在不同的谱系中,形成翅膀的基因网络有很大的差异。因此,尽管自然选择引导了表型趋同,但两个主要Heliconius谱系之间不同的发育环境开辟了不同的发育途径来进化相似性。因此,即使在非常确定的进化情景下,我们的结果也强调了在近期辐射趋同的发展路径中令人惊讶的不可预测性。
To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Mullerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5-4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three comimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the comimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation.