哺乳动物功能基因的适应性进化—回声定位鲸Cldn14基因与食虫蝙蝠RNASE1基因复制的研究
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摘要
本论文从两个方面探讨了哺乳动物生存的适应性进化机制,一方面是研究鲸和蝙蝠回声定位的分子适应性进化机制,另一方面是研究蝙蝠食性的分子适应性机制。继之前关于Prestin, Kcnq4, Chrna10, AGT, GLUT4等基因的研究,此论文又丰富了关于鲸及蝙蝠生理习性的研究。
鲸偶蹄目中的齿鲸和翼手目中的小蝙蝠两大哺乳动物类群分别独立地进化出发达的回声定位能力,并利用它辨别方向和捕捉食物。本论文的第一部分探讨鲸和蝙蝠听觉的适应性进化机制。近来的研究发现包括Prestin, Tme1, Pjvk,和Kcnq4等基因在回声定位鲸和蝙蝠内部都发生了适应性进化。该论文研究了听觉基因Cldn14,它编码的claudin-14蛋白是紧密连接蛋白的成员之一,对维持耳蜗内电位发挥重要的功能。该基因突变将会导致人类非综合征型耳聋,因此推测Cldn14基因在回声定位鲸和蝙蝠中具有重要的功能。此研究通过分子克隆实验和数据库搜索总共获得了8种鲸和4种蝙蝠的Cldn14基因序列,然后通过BLAT工具在Ensemb1和NCBI数据库中又获得了其它20个哺乳动物的序列。选择压力分析发现Cldn14基因在齿鲸内部发生了两次正选择,一次发生在所有齿鲸的祖先位置,另一次发生在delphinid, phocoenid和ziphiid的祖先位置。相关性分析证明鲸的超声频率大小与Cldn14基因的非同义替代数呈显著正相关,而与同义替代数没有相关性。这一发现正好与Prestin基因在鲸中的发现一致。但是与Prestin基因不同的是,Cldn14基因在蝙蝠类群中并没有发生正选择。综合Prestin基因与Cldnl4基因的研究表明,鲸回声定位的进化是由多基因协调作用发生的,同时也表明鲸和蝙蝠回声定位功能可能具有不同的分子基础。
蝙蝠食性非常广泛,包括食果和食虫等。本论文的第二部分探讨蝙蝠食性的分子进化机制。胰腺核糖核酸酶(RNASE1)在一些前肠发酵动物中,包括反刍动物和灵长类叶猴,发生了基因复制和适应性进化。另外,RNASE1在一些食肉动物中也发生了基因复制,推测它可能与食性相关。本研究通过分子克隆方法,并通过NCBI和Ensemb1数据库总共获得了24种蝙蝠的RNASE1序列,结果发现RNASE1基因在蝙蝠科和犬吻蝠科7种食虫蝙蝠中发生了大规模基因复制,每个物种具有两个或更多的拷贝,并且发现了3条假基因。贝叶斯法和最大似然法重建的系统发育树表明RNASE1基因在两个科内独立发生了基因复制。选择压力分析发现复制的RNASE1拷贝发生了正选择,这很可能与该基因功能的变化相关,并且在Tadarida β支系有显著的加速进化发生。然而,与其它哺乳动物RNase1蛋白的消化功能不同,蝙蝠RNASE1基因等电点相对较高,这可能是与消化双链RNA发挥免疫功能相关。本研究虽然没有发现RNASE1与食性的关系,但是发现RNASE1在食虫蝙蝠中发生了适应性进化,更多的实验需要进一步研究该酶在蝙蝠中的生理功能。
We discussed the adaptive evolution of mammals based on two aspects. One is about the mechanisms of echolocation in whales and bats, the other is on the molecular adaptive evolution of bats dietary switch. After the previous investigation on genes including Prestin, Kcnq4, Chrna10, AGT and GLUT4, we add more examples on molecular adaptive evolution in mammals.
Toothed whales and bats have independently evolved specialized ultrasonic hearing for echolocation. Recent findings have suggested that several genes including Prestin, Tmcl, Pjvk and Kcnq4appear to have undergone molecular adaptations associated with the evolution of this ultrasonic hearing in mammals. Here we studied the hearing gene Cldn14, which encodes the claudin-14protein and is a member of tight junction proteins that functions in the organ of Corti in the inner ear to maintain a cationic gradient between endolymph and perilymph. Particular mutations in human claudin-14give rise to non-syndromic deafness, suggesting an essential role in hearing. Our results uncovered two bursts of positive selection, one in the ancestral branch of all toothed whales and a second in the branch leading to the delphinid, phocoenid and ziphiid whales. These two branches are the same as those previously reported to show positive selection in the Prestin gene. Furthermore, as with Prestin, the estimated hearing frequencies of whales significantly correlate with numbers of branch-wise non-synonymous substitutions in Cldn14, but not with synonymous changes. However, in contrast to Prestin, we found no evidence of positive selection in bats. Our findings from Cldn14, and comparisons with Prestin, strongly implicate multiple loci in the acquisition of echolocation in cetaceans, but also highlight possible differences in the evolutionary route to echolocation taken by whales and bats.
Pancreatic ribonuclease gene (RNASE1) was previously shown to have undergone duplication and adaptive evolution related to digestive efficiency in several mammalian groups that have evolved foregut fermentation, including ruminants and some primates. RNASE1gene duplications thought to be linked to diet have also been recorded in some carnivores. Of all mammals, bats have evolved the most diverse dietary specializations, mainly including frugivory and insectivory. Here we cloned, sequenced and analysed KNASE1gene sequences from a range of bat species to determine whether their dietary adaptation is mirrored by molecular adaptation. We found that seven insect-eating members of the families Vespertilionidae and Molossidae possessed two or more duplicates, and we also detected three pseudogenes. Reconstructed RNASE1gene trees based on both Bayesian and maximum likelihood methods supported independent duplication events in these two families. Selection tests revealed that RNASE1gene duplicates have undergone episodes of positive selection indicative of functional modification, and lineage-specific tests revealed strong adaptive evolution in the Tadarida β clade. However, unlike the RNASE1duplicates that function in digestion in some mammals, the bat RNASE1sequences were found to be characterised by relatively high isoelectric points, a feature previously suggested to promote defense against viruses via the breakdown of double-stranded RNA. Taken together, our findings point to an adaptive diversification of RNASE1in these two bat families, although we find no clear evidence that this was driven by diet. Future experimental assays are needed to resolve the functions of these enzymes in bats.
鲸偶蹄目中的齿鲸和翼手目中的小蝙蝠两大哺乳动物类群分别独立地进化出发达的回声定位能力,并利用它辨别方向和捕捉食物。本论文的第一部分探讨鲸和蝙蝠听觉的适应性进化机制。近来的研究发现包括Prestin, Tme1, Pjvk,和Kcnq4等基因在回声定位鲸和蝙蝠内部都发生了适应性进化。该论文研究了听觉基因Cldn14,它编码的claudin-14蛋白是紧密连接蛋白的成员之一,对维持耳蜗内电位发挥重要的功能。该基因突变将会导致人类非综合征型耳聋,因此推测Cldn14基因在回声定位鲸和蝙蝠中具有重要的功能。此研究通过分子克隆实验和数据库搜索总共获得了8种鲸和4种蝙蝠的Cldn14基因序列,然后通过BLAT工具在Ensemb1和NCBI数据库中又获得了其它20个哺乳动物的序列。选择压力分析发现Cldn14基因在齿鲸内部发生了两次正选择,一次发生在所有齿鲸的祖先位置,另一次发生在delphinid, phocoenid和ziphiid的祖先位置。相关性分析证明鲸的超声频率大小与Cldn14基因的非同义替代数呈显著正相关,而与同义替代数没有相关性。这一发现正好与Prestin基因在鲸中的发现一致。但是与Prestin基因不同的是,Cldn14基因在蝙蝠类群中并没有发生正选择。综合Prestin基因与Cldnl4基因的研究表明,鲸回声定位的进化是由多基因协调作用发生的,同时也表明鲸和蝙蝠回声定位功能可能具有不同的分子基础。
蝙蝠食性非常广泛,包括食果和食虫等。本论文的第二部分探讨蝙蝠食性的分子进化机制。胰腺核糖核酸酶(RNASE1)在一些前肠发酵动物中,包括反刍动物和灵长类叶猴,发生了基因复制和适应性进化。另外,RNASE1在一些食肉动物中也发生了基因复制,推测它可能与食性相关。本研究通过分子克隆方法,并通过NCBI和Ensemb1数据库总共获得了24种蝙蝠的RNASE1序列,结果发现RNASE1基因在蝙蝠科和犬吻蝠科7种食虫蝙蝠中发生了大规模基因复制,每个物种具有两个或更多的拷贝,并且发现了3条假基因。贝叶斯法和最大似然法重建的系统发育树表明RNASE1基因在两个科内独立发生了基因复制。选择压力分析发现复制的RNASE1拷贝发生了正选择,这很可能与该基因功能的变化相关,并且在Tadarida β支系有显著的加速进化发生。然而,与其它哺乳动物RNase1蛋白的消化功能不同,蝙蝠RNASE1基因等电点相对较高,这可能是与消化双链RNA发挥免疫功能相关。本研究虽然没有发现RNASE1与食性的关系,但是发现RNASE1在食虫蝙蝠中发生了适应性进化,更多的实验需要进一步研究该酶在蝙蝠中的生理功能。
We discussed the adaptive evolution of mammals based on two aspects. One is about the mechanisms of echolocation in whales and bats, the other is on the molecular adaptive evolution of bats dietary switch. After the previous investigation on genes including Prestin, Kcnq4, Chrna10, AGT and GLUT4, we add more examples on molecular adaptive evolution in mammals.
Toothed whales and bats have independently evolved specialized ultrasonic hearing for echolocation. Recent findings have suggested that several genes including Prestin, Tmcl, Pjvk and Kcnq4appear to have undergone molecular adaptations associated with the evolution of this ultrasonic hearing in mammals. Here we studied the hearing gene Cldn14, which encodes the claudin-14protein and is a member of tight junction proteins that functions in the organ of Corti in the inner ear to maintain a cationic gradient between endolymph and perilymph. Particular mutations in human claudin-14give rise to non-syndromic deafness, suggesting an essential role in hearing. Our results uncovered two bursts of positive selection, one in the ancestral branch of all toothed whales and a second in the branch leading to the delphinid, phocoenid and ziphiid whales. These two branches are the same as those previously reported to show positive selection in the Prestin gene. Furthermore, as with Prestin, the estimated hearing frequencies of whales significantly correlate with numbers of branch-wise non-synonymous substitutions in Cldn14, but not with synonymous changes. However, in contrast to Prestin, we found no evidence of positive selection in bats. Our findings from Cldn14, and comparisons with Prestin, strongly implicate multiple loci in the acquisition of echolocation in cetaceans, but also highlight possible differences in the evolutionary route to echolocation taken by whales and bats.
Pancreatic ribonuclease gene (RNASE1) was previously shown to have undergone duplication and adaptive evolution related to digestive efficiency in several mammalian groups that have evolved foregut fermentation, including ruminants and some primates. RNASE1gene duplications thought to be linked to diet have also been recorded in some carnivores. Of all mammals, bats have evolved the most diverse dietary specializations, mainly including frugivory and insectivory. Here we cloned, sequenced and analysed KNASE1gene sequences from a range of bat species to determine whether their dietary adaptation is mirrored by molecular adaptation. We found that seven insect-eating members of the families Vespertilionidae and Molossidae possessed two or more duplicates, and we also detected three pseudogenes. Reconstructed RNASE1gene trees based on both Bayesian and maximum likelihood methods supported independent duplication events in these two families. Selection tests revealed that RNASE1gene duplicates have undergone episodes of positive selection indicative of functional modification, and lineage-specific tests revealed strong adaptive evolution in the Tadarida β clade. However, unlike the RNASE1duplicates that function in digestion in some mammals, the bat RNASE1sequences were found to be characterised by relatively high isoelectric points, a feature previously suggested to promote defense against viruses via the breakdown of double-stranded RNA. Taken together, our findings point to an adaptive diversification of RNASE1in these two bat families, although we find no clear evidence that this was driven by diet. Future experimental assays are needed to resolve the functions of these enzymes in bats.
引文
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