McFarland Emily P, Crow Karen D
University of California, San Diego, USA.
San Francisco State University, San Francisco, USA.
Evodevo. 2024 Dec 27;15(1):17. doi: 10.1186/s13227-024-00233-3.
Batoids possess a unique body plan associated with a benthic lifestyle that includes dorsoventral compression and anteriorly expanded pectoral fins that fuse to the rostrum. The family Myliobatidae, including manta rays and their relatives, exhibit further modifications associated with invasion of the pelagic environment, and the evolution of underwater flight. Notably, the pectoral fins are split into two domains with independent functions that are optimized for feeding and oscillatory locomotion. Paired fin outgrowth is maintained during development by Wnt3, while domain splitting is accomplished by expression of the Wnt antagonist Dkk1, which is differentially expressed in the developing anterior pectoral fins of myliobatids, where cephalic fins separate from pectoral fins. We examine the evolution of this unique feature in the cownose ray (Rhinoptera bonasus), a member of the genus that is sister to Mobula.
Here, we provide functional evidence that DKK1 is sufficient to initiate pectoral fin domain splitting. Agarose beads soaked in DKK1 protein were implanted in the pectoral fins of little skate (Leucoraja erinacea) embryos resulting in AER interruption. This disruption arrests fin ray outgrowth, resembling the myliobatid phenotype. In addition, fins that received DKK1 beads exhibit interruption of Axin2 expression, a downstream target of β-catenin-dependent Wnt signaling and a known AER marker. We demonstrate that Msx1 and Lhx2 are also associated with fin expansion at the AER. These results provide functional evidence for the underlying genetic pathway associated with the evolution of a novel paired fin/limb modification in manta rays and their relatives. We introduce the gas/brake pedal model for paired fin remodeling at the AER, which may have been co-opted from domain splitting in pelvic fins of cartilaginous fishes 370 million years earlier.
The pectoral fins of manta rays and their relatives represent a dramatic remodel of the ancestral batoid body plan. The premiere feature of this remodel is the cephalic fins, which evolved via domain splitting of the anterior pectoral fins through inhibition of fin ray outgrowth. Here, we functionally validate the role of Dkk1 in the evolution of this phenotype. We find that introduction of ectopic DKK1 is sufficient to recapitulate the myliobatid pectoral fin phenotype in an outgroup lacking cephalic fins via AER interruption and fin ray truncation. Additional gene expression data obtained via in situ hybridization suggests that cephalic fin development may have evolved as a co-option of the pathway specifying claspers as modifications to the pelvic fins, the only other known example of domain splitting in vertebrate appendages.
魟类具有与底栖生活方式相关的独特身体结构，包括背腹压缩以及与吻部融合的向前扩展的胸鳍。鲼科，包括蝠鲼及其近亲，表现出与远洋环境入侵以及水下飞行进化相关的进一步形态变化。值得注意的是，胸鳍分为两个具有独立功能的区域，分别针对捕食和摆动运动进行了优化。在发育过程中，Wnt3维持成对鳍的生长，而区域分裂则通过Wnt拮抗剂Dkk1的表达来实现，Dkk1在鲼科动物发育中的前胸鳍中差异表达，在那里头鳍与胸鳍分离。我们研究了牛鼻鲼（Rhinoptera bonasus）这一与蝠鲼属为姐妹群的属中的这一独特特征的进化。
在这里，我们提供了功能证据，证明DKK1足以启动胸鳍区域分裂。将浸泡在DKK1蛋白中的琼脂糖珠植入小斑鳐（Leucoraja erinacea）胚胎的胸鳍中，导致顶外胚层嵴（AER）中断。这种破坏阻止了鳍条的生长，类似于鲼科动物的表型。此外，接受DKK1珠的鳍显示出Axin2表达的中断，Axin2是β-连环蛋白依赖性Wnt信号的下游靶点，也是已知的AER标记物。我们证明Msx1和Lhx2也与AER处的鳍扩展有关。这些结果为与蝠鲼及其近亲中一种新型成对鳍/肢体形态变化进化相关的潜在遗传途径提供了功能证据。我们引入了AER处成对鳍重塑的气体/刹车踏板模型，这可能是从3.7亿年前软骨鱼类腹鳍的区域分裂中演变而来的。
蝠鲼及其近亲的胸鳍代表了祖先魟类身体结构的显著重塑。这种重塑的首要特征是头鳍，它是通过抑制鳍条生长使前胸鳍区域分裂而进化而来的。在这里，我们在功能上验证了Dkk1在这种表型进化中的作用。我们发现，通过AER中断和鳍条截断，引入异位DKK1足以在缺乏头鳍的外类群中重现鲼科动物的胸鳍表型。通过原位杂交获得的额外基因表达数据表明头鳍的发育可能是作为指定交合突作为腹鳍形态变化的途径的一种选择而进化的，这是脊椎动物附肢中区域分裂的另一个已知例子。
