鸟类对高海拔环境的适应性演化:从表型到基因组
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摘要
解析鸟类对高海拔高寒、低氧与强紫外辐射等极端环境的适应性状与遗传基础一直是演化生物学和群体遗传学的重点研究内容.在表型上,比较形态与生理学等方法揭示了高海拔鸟类形态、飞行能力以及血液生理等特征发生了显著变化.在基因型上,与氧运输和氧利用相关基因(如血红蛋白基因、细胞色素C氧化酶基因等)在高海拔鸟类中发生了适应性演化,进而改变相应蛋白的功能以适应低氧生存.近年随着高通量测序技术的发展,大规模比较基因组与转录组分析正逐步揭示鸟类高海拔适应的遗传机制.尽管传统手段与测序技术从不同角度揭示了鸟类高海拔适应方式,但当前仍缺乏对高海拔适应性状与遗传机制的系统性分析,尤其是在解析高寒低氧环境鸟类能量代谢策略上更加滞后;同时对涉及表型可塑性的复杂性状遗传解析也是当前的一大难题.因此,整合传统与各种组学手段,引入功能实验与同质园实验将会更高效、彻底地破译鸟类高海拔适应性状的遗传基础,这也是未来解析鸟类高海拔适应的研究趋势.
In the field of evolutionary biology and population genetics,the revealing of the genetic basis of adaptation in birds in response to extreme environmental conditions in highlands(e.g.,hypothermia,hypoxia,and high UV radiation) is an interesting study topic.Previous studies based on comparative morphological and physiological analyses have revealed that body size,flight ability,and hematology are significantly altered in high-altitude birds.Some genes associated with oxygen transport and utilization(e.g.,hemoglobin and cytochrome coxidase) are reportedly involved in hypoxic responses and could facilitate adaptive hypoxic evolution.Next-generation sequencing techniques applied in highland adaptation research,comparative genome analyses,and transcriptome analyses are revealing the genetic mechanisms underlying numerous complex traits.However,systematic studies based on adaptive phenotypes and molecular methods are unreliable,particularly in investigating bird metabolism under hypoxic cold stress,which remains largely unclear to date.In addition,the influence of phenotypic plasticity on some geographical variations in complex traits poses a challenge in highland adaptation studies.Therefore,the integration of traditional methods and sequencing techniques,in combination with functional and common garden experiments is essential for a comprehensive understanding of the genetic basis of such complex traits,which are interesting key topics of study on avian highland adaptation.
In the field of evolutionary biology and population genetics,the revealing of the genetic basis of adaptation in birds in response to extreme environmental conditions in highlands(e.g.,hypothermia,hypoxia,and high UV radiation) is an interesting study topic.Previous studies based on comparative morphological and physiological analyses have revealed that body size,flight ability,and hematology are significantly altered in high-altitude birds.Some genes associated with oxygen transport and utilization(e.g.,hemoglobin and cytochrome coxidase) are reportedly involved in hypoxic responses and could facilitate adaptive hypoxic evolution.Next-generation sequencing techniques applied in highland adaptation research,comparative genome analyses,and transcriptome analyses are revealing the genetic mechanisms underlying numerous complex traits.However,systematic studies based on adaptive phenotypes and molecular methods are unreliable,particularly in investigating bird metabolism under hypoxic cold stress,which remains largely unclear to date.In addition,the influence of phenotypic plasticity on some geographical variations in complex traits poses a challenge in highland adaptation studies.Therefore,the integration of traditional methods and sequencing techniques,in combination with functional and common garden experiments is essential for a comprehensive understanding of the genetic basis of such complex traits,which are interesting key topics of study on avian highland adaptation.
引文
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2 Monge C,León-Velarde F.Physiological adaptation to high altitude:Oxygen transport in mammals and birds.Physiol Rev,1991,71:1135-1172
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4 Riemer K,Guralnick R P,White E P.No general relationship between mass and temperature in endothermic species.e Life,2018,7:e27166
5 Shao S,Quan Q,Cai T,et al.Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 paridae species.Front Zool,2016,13:30
6 Sun Y M,Li M,Song G,et al.The role of climate factors in geographic variation in body mass and wing length in a passerine bird.Avian Res,2017,8:1
7 Altshuler D L,Dudley R.The physiology and biomechanics of avian flight at high altitude.Integr Comp Biol,2006,46:62-71
8 Dudley R,Chai P.Animal flight mechanics in physically variable gas mixtures.J Exp Biol,1996,199:1881-1885
9 Sun Y F,Ren Z P,Wu Y F,et al.Flying high:Limits to flight performance by sparrows on the qinghai-tibet plateau.J Exp Biol,2016,219:3642-3648
10 Storz J F,Scott G R,Cheviron Z A.Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates.J Exp Biol,2010,213:4125-4136
11 Scheid P.Avian Respiratory System and Gas Exchange.Hypoxia:The Adaptations,1990.4-7
12 Barve S,Dhondt A A,Mathur V B,et al.Life-history characteristics influence physiological strategies to cope with hypoxia in himalayan birds.Proc R Soc B,2016,283:20162201
13 Scott G R,Egginton S,Richards J G,et al.Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose.Proc R Soc B,2009,276:3645-3653
14 Scott G R,Schulte P M,Egginton S,et al.Molecular evolution of cytochrome C oxidase underlies high-altitude adaptation in the bar-headed goose.Mol Biol Evol,2011,28:351-363
15 Scott G R,Milsom W K.Control of breathing and adaptation to high altitude in the bar-headed goose.Am J Physiol-Reg Integr Comp Physiol,2007,293:R379-R391
16 York J M,Chua B A,Ivy C M,et al.Respiratory mechanics of eleven avian species resident at high and low altitude.J Exp Biol,2017,220:1079-1089
17 Dawson N J,Ivy C M,Alza L,et al.Mitochondrial physiology in the skeletal and cardiac muscles is altered in torrent ducks,Merganetta armata,from high altitudes in the Andes.J Exp Biol,2016,219:3719-3728
18 Beall C M,Cavalleri G L,Deng L,et al.Natural selection on EPAS1(HIF2α)associated with low hemoglobin concentration in Tibetan highlanders.Proc Natl Acad Sci USA,2010,107:11459-11464
19 Yi X,Liang Y,Huerta-Sanchez E,et al.Sequencing of 50 human exomes reveals adaptation to high altitude.Science,2010,329:75-78
20 Xu S H,Li S L,Yang Y J,et al.A genome-wide search for signals of high-altitude adaptation in tibetans.Mol Biol Evol,2011,28:1003-1011
21 Simonson T S,Yang Y Z,Huff C D,et al.Genetic evidence for high-altitude adaptation in Tibet.Science,2010,329:72-75
22 Rich P.Chemiosmotic coupling:The cost of living.Nature,2003,421:583
23 Luo Y J,Gao W X,Liu F Y,et al.Mitochondrial nt3010G-nt3970C haplotype is implicated in high-altitude adaptation of tibetans.Mitochondr DNA,2011,22:181-190
24 Gu M L,Dong X Q,Shi L,et al.Differences in mt DNA whole sequence between tibetan and Han populations suggesting adaptive selection to high altitude.Gene,2012,496:37-44
25 da Fonseca R R,Johnson W E,O’Brien S J,et al.The adaptive evolution of the mammalian mitochondrial genome.BMC Genomics,2008,9:119
26 Lau G Y,Mandic M,Richards J G.Evolution of cytochrome C oxidase in hypoxia tolerant sculpins(Cottidae,Actinopterygii).Mol Biol Evol,2017,34:2153-2162
27 Aon M A,Cortassa S,O’Rourke B.Redox-optimized ros balance:A unifying hypothesis.Biochim Biophys Acta(BBA)-Bioenerg,2010,1797:865-877
28 Dosek A,Ohno H,Acs Z,et al.High altitude and oxidative stress.Resp Physiol Neurobiol,2007,158:128-131
29 Brown J C L,Mc Clelland G B,Faure P A,et al.Examining the mechanisms responsible for lower ROS release rates in liver mitochondria from the long-lived house sparrow(Passer domesticus)and big brown bat(Eptesicus fuscus)compared to the short-lived mouse(Mus musculus).Mech Ageing Dev,2009,130:467-476
30 Weber R E,Fago A.Functional adaptation and its molecular basis in vertebrate hemoglobins,neuroglobins and cytoglobins.Resp Physiol Neurobiol,2004,144:141-159
31 Storz J F,Moriyama H.Mechanisms of hemoglobin adaptation to high altitude hypoxia.High Altitude Med Biol,2008,9:148-157
32 Projecto-Garcia J,Natarajan C,Moriyama H,et al.Repeated elevational transitions in hemoglobin function during the evolution of andean hummingbirds.Proc Natl Acad Sci USA,2013,110:20669-20674
33 Galen S C,Natarajan C,Moriyama H,et al.Contribution of a mutational hot spot to hemoglobin adaptation in high-altitude andean house wrens.Proc Natl Acad Sci USA,2015,112:13958-13963
34 Natarajan C,Hoffmann F G,Weber R E,et al.Predictable convergence in hemoglobin function has unpredictable molecular underpinnings.Science,2016,354:336-339
35 Stoltzfus A,Mc Candlish D M.Mutation-biased adaptation in andean house wrens.Proc Natl Acad Sci USA,2015,112:13753-13754
36 Natarajan C,Projecto-Garcia J,Moriyama H,et al.Convergent evolution of hemoglobin function in high-altitude andean waterfowl involves limited parallelism at the molecular sequence level.PLo S Genet,2015,11:e1005681
37 Zhu X J,Guan Y Y,Signore AV,et al.Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the QinghaiTibet Plateau.Proc Natl Acad Sci USA,2018,115:1865-1870
38 Zhu X J,Guan Y Y,Qu Y H,et al.Elevational divergence in the great tit complex revealed by major hemoglobin genes.Curr Zool,2018,64:455-464
39 Qu Y H,Zhao H W,Han N J,et al.Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan Plateau.Nat Commun,2013,4:2071
40 Wang M S,Li Y,Peng M S,et al.Genomic analyses reveal potential independent adaptation to high altitude in tibetan chickens.Mol Biol Evol,2015,32:1880-1889
41 Li M Z,Tian S L,Jin L,et al.Genomic analyses identify distinct patterns of selection in domesticated pigs and tibetan wild boars.Nat Genet,2013,45:1431-1438
42 Qiu Q,Zhang G J,Ma T,et al.The yak genome and adaptation to life at high altitude.Nat Genet,2012,44:946-949
43 Cheviron Z A,Bachman G C,Connaty A D,et al.Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in highaltitude deer mice.Proc Natl Acad Sci USA,2012,109:8635-8640
44 Zhang Q,Gou W Y,Wang X T,et al.Genome resequencing identifies unique adaptations of tibetan chickens to hypoxia and high-dose ultraviolet radiation in high-altitude environments.Genome Biol Evol,2016,8:765-776
45 Qu Y,Tian S L,Han N J,et al.Genetic responses to seasonal variation in altitudinal stress:Whole-genome resequencing of great tit in eastern Himalayas.Sci Rep,2015,5:14256
46 Cheng Y L,Gao B,Wang H T,et al.Evolution of beak morphology in the ground tit revealed by comparative transcriptomics.Front Zool,2017,14:58
47 Chen X M,Qu Y H,Cheng Y L,et al.Mi R-19b-3p regulates MAPK1 expression in embryonic fibroblasts from the great tit(Parus major)under hypoxic conditions.Cell Physiol Biochem,2018,46:546-560
48 Cheviron Z A,Whitehead A,Brumfield R T.Transcriptomic variation and plasticity in rufous-collared sparrows(Zonotrichia capensis)along an altitudinal gradient.Mol Ecol,2008,17:4556-4569
49 Schippers M P,Ramirez O,Arana M,et al.Increase in carbohydrate utilization in high-altitude andean mice.Curr Biol,2012,22:2350-2354
50 Horscroft J A,Kotwica A O,Laner V,et al.Metabolic basis to sherpa altitude adaptation.Proc Natl Acad Sci USA,2017,114:6382-6387
51 Cheviron Z A,Swanson D L.Comparative transcriptomics of seasonal phenotypic flexibility in two north american songbirds.Integr Comp Biol,2017,57:1040-1054
52 Sultan S E.Phenotypic plasticity and plant adaptation.Acta Bot Neerl,1995,44:363-383
53 Savolainen O,Lascoux M,Meril?J.Ecological genomics of local adaptation.Nat Rev Genet,2013,14:807-820
54 Scott G R,Elogio T S,Lui M A,et al.Adaptive modifications of muscle phenotype in high-altitude deer mice are associated with evolved changes in gene regulation.Mol Biol Evol,2015,32:1962-1976
2 Monge C,León-Velarde F.Physiological adaptation to high altitude:Oxygen transport in mammals and birds.Physiol Rev,1991,71:1135-1172
3 Cheviron Z A,Natarajan C,Projecto-Garcia J,et al.Integrating evolutionary and functional tests of adaptive hypotheses:A case study of altitudinal differentiation in hemoglobin function in an andean sparrow,zonotrichia capensis.Mol Biol Evol,2014,31:2948-2962
4 Riemer K,Guralnick R P,White E P.No general relationship between mass and temperature in endothermic species.e Life,2018,7:e27166
5 Shao S,Quan Q,Cai T,et al.Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 paridae species.Front Zool,2016,13:30
6 Sun Y M,Li M,Song G,et al.The role of climate factors in geographic variation in body mass and wing length in a passerine bird.Avian Res,2017,8:1
7 Altshuler D L,Dudley R.The physiology and biomechanics of avian flight at high altitude.Integr Comp Biol,2006,46:62-71
8 Dudley R,Chai P.Animal flight mechanics in physically variable gas mixtures.J Exp Biol,1996,199:1881-1885
9 Sun Y F,Ren Z P,Wu Y F,et al.Flying high:Limits to flight performance by sparrows on the qinghai-tibet plateau.J Exp Biol,2016,219:3642-3648
10 Storz J F,Scott G R,Cheviron Z A.Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates.J Exp Biol,2010,213:4125-4136
11 Scheid P.Avian Respiratory System and Gas Exchange.Hypoxia:The Adaptations,1990.4-7
12 Barve S,Dhondt A A,Mathur V B,et al.Life-history characteristics influence physiological strategies to cope with hypoxia in himalayan birds.Proc R Soc B,2016,283:20162201
13 Scott G R,Egginton S,Richards J G,et al.Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose.Proc R Soc B,2009,276:3645-3653
14 Scott G R,Schulte P M,Egginton S,et al.Molecular evolution of cytochrome C oxidase underlies high-altitude adaptation in the bar-headed goose.Mol Biol Evol,2011,28:351-363
15 Scott G R,Milsom W K.Control of breathing and adaptation to high altitude in the bar-headed goose.Am J Physiol-Reg Integr Comp Physiol,2007,293:R379-R391
16 York J M,Chua B A,Ivy C M,et al.Respiratory mechanics of eleven avian species resident at high and low altitude.J Exp Biol,2017,220:1079-1089
17 Dawson N J,Ivy C M,Alza L,et al.Mitochondrial physiology in the skeletal and cardiac muscles is altered in torrent ducks,Merganetta armata,from high altitudes in the Andes.J Exp Biol,2016,219:3719-3728
18 Beall C M,Cavalleri G L,Deng L,et al.Natural selection on EPAS1(HIF2α)associated with low hemoglobin concentration in Tibetan highlanders.Proc Natl Acad Sci USA,2010,107:11459-11464
19 Yi X,Liang Y,Huerta-Sanchez E,et al.Sequencing of 50 human exomes reveals adaptation to high altitude.Science,2010,329:75-78
20 Xu S H,Li S L,Yang Y J,et al.A genome-wide search for signals of high-altitude adaptation in tibetans.Mol Biol Evol,2011,28:1003-1011
21 Simonson T S,Yang Y Z,Huff C D,et al.Genetic evidence for high-altitude adaptation in Tibet.Science,2010,329:72-75
22 Rich P.Chemiosmotic coupling:The cost of living.Nature,2003,421:583
23 Luo Y J,Gao W X,Liu F Y,et al.Mitochondrial nt3010G-nt3970C haplotype is implicated in high-altitude adaptation of tibetans.Mitochondr DNA,2011,22:181-190
24 Gu M L,Dong X Q,Shi L,et al.Differences in mt DNA whole sequence between tibetan and Han populations suggesting adaptive selection to high altitude.Gene,2012,496:37-44
25 da Fonseca R R,Johnson W E,O’Brien S J,et al.The adaptive evolution of the mammalian mitochondrial genome.BMC Genomics,2008,9:119
26 Lau G Y,Mandic M,Richards J G.Evolution of cytochrome C oxidase in hypoxia tolerant sculpins(Cottidae,Actinopterygii).Mol Biol Evol,2017,34:2153-2162
27 Aon M A,Cortassa S,O’Rourke B.Redox-optimized ros balance:A unifying hypothesis.Biochim Biophys Acta(BBA)-Bioenerg,2010,1797:865-877
28 Dosek A,Ohno H,Acs Z,et al.High altitude and oxidative stress.Resp Physiol Neurobiol,2007,158:128-131
29 Brown J C L,Mc Clelland G B,Faure P A,et al.Examining the mechanisms responsible for lower ROS release rates in liver mitochondria from the long-lived house sparrow(Passer domesticus)and big brown bat(Eptesicus fuscus)compared to the short-lived mouse(Mus musculus).Mech Ageing Dev,2009,130:467-476
30 Weber R E,Fago A.Functional adaptation and its molecular basis in vertebrate hemoglobins,neuroglobins and cytoglobins.Resp Physiol Neurobiol,2004,144:141-159
31 Storz J F,Moriyama H.Mechanisms of hemoglobin adaptation to high altitude hypoxia.High Altitude Med Biol,2008,9:148-157
32 Projecto-Garcia J,Natarajan C,Moriyama H,et al.Repeated elevational transitions in hemoglobin function during the evolution of andean hummingbirds.Proc Natl Acad Sci USA,2013,110:20669-20674
33 Galen S C,Natarajan C,Moriyama H,et al.Contribution of a mutational hot spot to hemoglobin adaptation in high-altitude andean house wrens.Proc Natl Acad Sci USA,2015,112:13958-13963
34 Natarajan C,Hoffmann F G,Weber R E,et al.Predictable convergence in hemoglobin function has unpredictable molecular underpinnings.Science,2016,354:336-339
35 Stoltzfus A,Mc Candlish D M.Mutation-biased adaptation in andean house wrens.Proc Natl Acad Sci USA,2015,112:13753-13754
36 Natarajan C,Projecto-Garcia J,Moriyama H,et al.Convergent evolution of hemoglobin function in high-altitude andean waterfowl involves limited parallelism at the molecular sequence level.PLo S Genet,2015,11:e1005681
37 Zhu X J,Guan Y Y,Signore AV,et al.Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the QinghaiTibet Plateau.Proc Natl Acad Sci USA,2018,115:1865-1870
38 Zhu X J,Guan Y Y,Qu Y H,et al.Elevational divergence in the great tit complex revealed by major hemoglobin genes.Curr Zool,2018,64:455-464
39 Qu Y H,Zhao H W,Han N J,et al.Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan Plateau.Nat Commun,2013,4:2071
40 Wang M S,Li Y,Peng M S,et al.Genomic analyses reveal potential independent adaptation to high altitude in tibetan chickens.Mol Biol Evol,2015,32:1880-1889
41 Li M Z,Tian S L,Jin L,et al.Genomic analyses identify distinct patterns of selection in domesticated pigs and tibetan wild boars.Nat Genet,2013,45:1431-1438
42 Qiu Q,Zhang G J,Ma T,et al.The yak genome and adaptation to life at high altitude.Nat Genet,2012,44:946-949
43 Cheviron Z A,Bachman G C,Connaty A D,et al.Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in highaltitude deer mice.Proc Natl Acad Sci USA,2012,109:8635-8640
44 Zhang Q,Gou W Y,Wang X T,et al.Genome resequencing identifies unique adaptations of tibetan chickens to hypoxia and high-dose ultraviolet radiation in high-altitude environments.Genome Biol Evol,2016,8:765-776
45 Qu Y,Tian S L,Han N J,et al.Genetic responses to seasonal variation in altitudinal stress:Whole-genome resequencing of great tit in eastern Himalayas.Sci Rep,2015,5:14256
46 Cheng Y L,Gao B,Wang H T,et al.Evolution of beak morphology in the ground tit revealed by comparative transcriptomics.Front Zool,2017,14:58
47 Chen X M,Qu Y H,Cheng Y L,et al.Mi R-19b-3p regulates MAPK1 expression in embryonic fibroblasts from the great tit(Parus major)under hypoxic conditions.Cell Physiol Biochem,2018,46:546-560
48 Cheviron Z A,Whitehead A,Brumfield R T.Transcriptomic variation and plasticity in rufous-collared sparrows(Zonotrichia capensis)along an altitudinal gradient.Mol Ecol,2008,17:4556-4569
49 Schippers M P,Ramirez O,Arana M,et al.Increase in carbohydrate utilization in high-altitude andean mice.Curr Biol,2012,22:2350-2354
50 Horscroft J A,Kotwica A O,Laner V,et al.Metabolic basis to sherpa altitude adaptation.Proc Natl Acad Sci USA,2017,114:6382-6387
51 Cheviron Z A,Swanson D L.Comparative transcriptomics of seasonal phenotypic flexibility in two north american songbirds.Integr Comp Biol,2017,57:1040-1054
52 Sultan S E.Phenotypic plasticity and plant adaptation.Acta Bot Neerl,1995,44:363-383
53 Savolainen O,Lascoux M,Meril?J.Ecological genomics of local adaptation.Nat Rev Genet,2013,14:807-820
54 Scott G R,Elogio T S,Lui M A,et al.Adaptive modifications of muscle phenotype in high-altitude deer mice are associated with evolved changes in gene regulation.Mol Biol Evol,2015,32:1962-1976