Department of Biology, University of California, Riverside, CA 92521, USA.
BMC Evol Biol. 2013 Jan 23;13:20. doi: 10.1186/1471-2148-13-20.
Secondary edentulism (toothlessness) has evolved on multiple occasions in amniotes including several mammalian lineages (pangolins, anteaters, baleen whales), birds, and turtles. All edentulous amniote clades have evolved from ancestors with enamel-capped teeth. Previous studies have documented the molecular decay of tooth-specific genes in edentulous mammals, all of which lost their teeth in the Cenozoic, and birds, which lost their teeth in the Cretaceous. By contrast with mammals and birds, tooth loss in turtles occurred in the Jurassic (201.6-145.5 Ma), providing an extended time window for tooth gene degradation in this clade. The release of the painted turtle and Chinese softshell turtle genomes provides an opportunity to recover the decayed remains of tooth-specific genes in Testudines.
We queried available genomes of Testudines (Chrysemys picta [painted turtle], Pelodiscus sinensis [Chinese softshell turtle]), Aves (Anas platyrhynchos [duck], Gallus gallus [chicken], Meleagris gallopavo [turkey], Melopsittacus undulatus [budgerigar], Taeniopygia guttata [zebra finch]), and enamelless mammals (Orycteropus afer [aardvark], Choloepus hoffmanni [Hoffmann's two-toed sloth], Dasypus novemcinctus [nine-banded armadillo]) for remnants of three enamel matrix protein (EMP) genes with putative enamel-specific functions. Remnants of the AMBN and ENAM genes were recovered in Chrysemys and retain their original synteny. Remnants of AMEL were recovered in both testudines, although there are no shared frameshifts. We also show that there are inactivated copies of AMBN, AMEL and ENAM in representatives of divergent avian lineages including Galloanserae, Passeriformes, and Psittaciformes, and that there are shared frameshift mutations in all three genes that predate the basal split in Neognathae. Among enamelless mammals, all three EMP genes exhibit inactivating mutations in Orycteropus and Choloepus.
Our results highlight the power of combining fossil and genomic evidence to decipher macroevolutionary transitions and characterize the functional range of different loci involved in tooth development. The fossil record and phylogenetics combine to predict the occurrence of molecular fossils of tooth-specific genes in the genomes of edentulous amniotes, and in every case these molecular fossils have been discovered. The widespread occurrence of EMP pseudogenes in turtles, birds, and edentulous/enamelless mammals also provides compelling evidence that in amniotes, the only unique, non-redundant function of these genes is in enamel formation.
次生缺齿（无齿）在羊膜动物中多次进化，包括几个哺乳动物谱系（穿山甲、食蚁兽、须鲸）、鸟类和海龟。所有无齿羊膜动物类群都从有釉质覆盖牙齿的祖先进化而来。先前的研究记录了无齿哺乳动物中特定于牙齿的基因的分子退化，所有这些哺乳动物在新生代都失去了牙齿，鸟类在白垩纪失去了牙齿。与哺乳动物和鸟类不同，海龟的牙齿缺失发生在侏罗纪（201.6-145.5 Ma），为这个类群的牙齿基因退化提供了一个更长的时间窗口。中华鳖和中华鳖基因组的发布为恢复龟鳖类特定于牙齿的基因的退化残骸提供了机会。
我们在 Testudines（Chrysemys picta[彩绘龟]、Pelodiscus sinensis[中华鳖]）、Aves（Anas platyrhynchos[鸭]、Gallus gallus[鸡]、Meleagris gallopavo[火鸡]、Melopsittacus undulatus[虎皮鹦鹉]、Taeniopygia guttata[斑马雀]）和无釉质哺乳动物（Orycteropus afer[土豚]、Choloepus hoffmanni[霍夫曼双趾树懒]、Dasypus novemcinctus[九带犰狳]）的可用基因组中查询了三个具有潜在釉质特异性功能的釉质基质蛋白（EMP）基因的残余物。AMBN 和 ENAM 基因的残余物在 Chrysemys 中被回收，并保留其原始的同线性。在两种龟鳖类中都回收了 AMEL 的残余物，尽管没有共享移码突变。我们还表明，在包括 Galloanserae、Passeriformes 和 Psittaciformes 在内的不同鸟类谱系中，存在 AMBN、AMEL 和 ENAM 的失活拷贝，并且在 Neognathae 的基础分裂之前，所有三个基因都存在共享的移码突变。在无釉质哺乳动物中，所有三种 EMP 基因在 Orycteropus 和 Choloepus 中都表现出失活突变。
我们的研究结果突出了结合化石和基因组证据来破译宏观进化转变和表征不同参与牙齿发育的基因功能范围的能力。化石记录和系统发育学相结合，预测了无齿羊膜动物基因组中特定于牙齿的基因的分子化石的出现，而且在每种情况下都发现了这些分子化石。EMP 假基因在龟鳖类、鸟类和无齿/无釉质哺乳动物中的广泛存在也提供了令人信服的证据，表明在羊膜动物中，这些基因的唯一独特、非冗余功能是在釉质形成中。
