Graduate Program in Organismic and Evolutionary Biology and.
Department of Biology, University of Massachusetts, Amherst, MA 01003
Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8530-4. doi: 10.1073/pnas.1323154111. Epub 2014 May 27.
Adaptive variation in the craniofacial skeleton is a key component of resource specialization and habitat divergence in vertebrates, but the proximate genetic mechanisms that underlie complex patterns of craniofacial variation are largely unknown. Here we demonstrate that the Hedgehog (Hh) signaling pathway mediates widespread variation across a complex functional system that affects the kinematics of lower jaw depression--the opercular four-bar linkage apparatus--among Lake Malawi cichlids. By using a combined quantitative trait locus mapping and population genetics approach, we show that allelic variation in the Hh receptor, ptch1, affects the development of distinct bony elements in the head that represent two of three movable links in this functional system. The evolutionarily derived allele is found in species that feed from the water column, and is associated with shifts in anatomy that translate to a four-bar system capable of faster jaw rotation. Alternatively, the ancestral allele is found in species that feed on attached algae, and is associated with the development of a four-bar system that predicts slower jaw movement. Experimental manipulation of the Hh pathway during cichlid development recapitulates functionally salient natural variation in craniofacial geometry. In all, these results significantly extend our understanding of the mechanisms that fine-tune the craniofacial skeletal complex during adaptation to new foraging niches.
颅面骨骼的适应性变异是脊椎动物资源特化和栖息地分化的关键组成部分，但导致颅面变异复杂模式的近因遗传机制在很大程度上仍是未知的。在这里，我们证明 Hedgehog（Hh）信号通路介导了广泛的变异，这些变异影响了马拉维湖慈鲷下颚下降的运动学——动耳肌四连杆联动装置——跨越了一个复杂的功能系统。通过使用定量性状定位和群体遗传学方法，我们表明 Hh 受体 ptch1 的等位基因变异影响了头部中两个可移动链接的三个中两个不同的骨骼元素的发育。在从水柱中觅食的物种中发现了进化衍生的等位基因，并且与解剖结构的转变相关，这些转变转化为能够实现更快的下颚旋转的四连杆系统。相比之下，在以附着藻类为食的物种中发现了祖先等位基因，并且与能够预测下颚运动较慢的四连杆系统的发育相关。在慈鲷发育过程中对 Hh 通路的实验操作再现了颅面几何形状的功能上显著的自然变异。总之，这些结果大大扩展了我们对在适应新觅食小生境过程中精细调整颅面骨骼复合体的机制的理解。
