Comparative Skin Histology of Frogs Reveals High-elevation Adaptation of the Tibetan Nanorana parkeri
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摘要
Adaptations to extreme environmental conditions are intriguing. Animal skin, which directly interacts with external environment, plays diverse and important roles in adaptive evolution. The thin and bare skin of amphibians is sensitive to external environmental conditions and, thus, it facilitates investigations into adaptations for living in extreme environments. Herein, we compare the structures of skin in four anuran species living at elevations ranging from 100 m to 4500 m to assess phenotypic innovations in the skin of Nanorana parkeri, which lives at extremely high elevations. Analyses reveal similar basic skin structures, but N. parkeri differs from the other species by having more epidermal capillaries and granular glands, which correlate highly with responses to hypoxia and/or ultraviolet(UV) radiation. Further intraspecific comparisons from frogs taken at ～4500 m and ～2900 m reveal that all of the changes are fixed. Changes occurring only in the higher elevation population, such as possessing more skin pigments, may represent local adaptations to coldness and/or UV radiation. These results provide a morphological basis for understanding further the molecular adaptations of these frogs.
Adaptations to extreme environmental conditions are intriguing. Animal skin, which directly interacts with external environment, plays diverse and important roles in adaptive evolution. The thin and bare skin of amphibians is sensitive to external environmental conditions and, thus, it facilitates investigations into adaptations for living in extreme environments. Herein, we compare the structures of skin in four anuran species living at elevations ranging from 100 m to 4500 m to assess phenotypic innovations in the skin of Nanorana parkeri, which lives at extremely high elevations. Analyses reveal similar basic skin structures, but N. parkeri differs from the other species by having more epidermal capillaries and granular glands, which correlate highly with responses to hypoxia and/or ultraviolet(UV) radiation. Further intraspecific comparisons from frogs taken at ～4500 m and ～2900 m reveal that all of the changes are fixed. Changes occurring only in the higher elevation population, such as possessing more skin pigments, may represent local adaptations to coldness and/or UV radiation. These results provide a morphological basis for understanding further the molecular adaptations of these frogs.
Adaptations to extreme environmental conditions are intriguing. Animal skin, which directly interacts with external environment, plays diverse and important roles in adaptive evolution. The thin and bare skin of amphibians is sensitive to external environmental conditions and, thus, it facilitates investigations into adaptations for living in extreme environments. Herein, we compare the structures of skin in four anuran species living at elevations ranging from 100 m to 4500 m to assess phenotypic innovations in the skin of Nanorana parkeri, which lives at extremely high elevations. Analyses reveal similar basic skin structures, but N. parkeri differs from the other species by having more epidermal capillaries and granular glands, which correlate highly with responses to hypoxia and/or ultraviolet(UV) radiation. Further intraspecific comparisons from frogs taken at ～4500 m and ～2900 m reveal that all of the changes are fixed. Changes occurring only in the higher elevation population, such as possessing more skin pigments, may represent local adaptations to coldness and/or UV radiation. These results provide a morphological basis for understanding further the molecular adaptations of these frogs.
引文
Brizzi R.,Delfino G.,Pellegrini R.2002.Specialized mucous glands and their possible adaptive role in the males of some species of Rana(Amphibia,Anura).J Morphol,254(3):328-341
Cao Y.,Xie F.,Jiang J.P.2011.Histological observation of skin in fourspecies in the genus Scutiger.Sichun J Zool,30(2):214-2119(In Chinese)
Che J.,Wang K.2016.AmphibiaChina:an online database of Chinese amphibians.Zool Res,37(1):57-59
Che J.,Zhou W.W.,Hu J.S.,Yan F.,Papenfuss T.J.,Wake D.B.,Zhang Y.P.2010.Spiny frogs(Paini)illuminate the history of the Himalayan region and Southeast Asia.Proc Natl Acad Sci U S A,107(31):13765-13770
Cheviron Z.A.,Brumfield R.T.2009.Migration-selection balance and local adaptation of mitochondrial haplotypes in rufouscollared sparrows(Zonotrichia capensis)along an elevational gradient.Evolution,63(6):1593-1605
Cheviron Z.A.,Connaty A.D.,McClelland G.B.,Storz J.F.2014.Functional genomics of adaptation to hypoxic coldstress in high-altitude deer mice:transcriptomic plasticity and thermogenic performance.Evolution,68(1):48-62
Del Bino S.,Bernerd F.2013.Variations in skin colour and the biological consequences of ultraviolet radiation exposure.Br JDermatol,169 Suppl 3:33-40
Delfino G.,Giachi F.,Malentacchi C.,Nosi D.2015.Ultrastructural evidence of serous gland polymorphism in the skin of the Tungara frog Engystomops pustulosus(Anura Leptodactylidae).Anat Rec(Hoboken),298(9):1659-1667
Denver R.J.2009.Stress hormones mediate environment-genotype interactions during amphibian development.Gen Comp Endocrinol,164(1):20-31
Fusco G.,Minelli A.2010.Phenotypic plasticity in development and evolution:facts and concepts.Philos Trans R Soc Lond BBiol Sci,365(1540):547-556
Greenberg N.M.,DeMayo F.,Finegold M.J.,Medina D.,Tilley W.D.,Aspinall J.O.,Cunha G.R.,Donjacour A.A.,Matusik R.J.,Rosen J.M.1995.Prostate cancer in a transgenic mouse.Proc Natl Acad Sci U S A,92(8):3439-3443
Hassanin A.,Ropiquet A.,Couloux A.,Cruaud C.2009.Evolution of the mitochondrial genome in mammals living at high altitude:new insights from a study of the tribe Caprini(Bovidae,Antilopinae).J Mol Evol,68(4):293-310
Huang L.,Li J.,Anboukaria H.,Luo Z.,Zhao M.,Wu H.2016.Comparative transcriptome analyses of seven anurans reveal functions and adaptations of amphibian skin.Sci Rep,6:24069
Jablonski N.G.,Chaplin G.2010.Colloquium paper:human skin pigmentation as an adaptation to UV radiation.Proc Natl Acad Sci U S A,107 Suppl 2:8962-8968
Jia L.L.,Tian C.,Li S.L.2013.Comparative histologial observation of skin in male and female frog(Rana dybouwskii)during breeding season.Chinese Agri Sci Bull,29(2):23-26(In Chinese)
Kim D.S.,Park S.H.,Kwon S.B.,Youn S.W.,Park E.S.,Park K.C.2005.Heat treatment decreases melanin synthesis via protein phosphatase 2A inactivation.Cell Signal,17(8):1023-1031
Liang G.,Wang Q.X.2004.Histological characteristics of the skin and cutaneous glands in Paa quadranus.Chin J Zool,39(4):73-76(In Chinese)
Ma X.Y.,Lu X.2010.Annual cycle of reproductive organs in a Tibetan frog,Nanorana parkeri.Anim Biol,60(3):259-271
Melzer S.,Clerens S.,Bishop P.J.2013.Skin gland morphology and secretory peptides in naturalized Litoria species in New Zealand.J Herpetol,47(4):565-574
Mi Z.P.,Liao W.B.2016.Comparison of skin histostructures in three species of genus Rana.Chin J Zool,51(5):844-852(In Chinese)
Norsang G.,Kocbach L.,Stamnes J.,Tsoja W.2011.Spatial distribution and temporal variation of solar UV radiation over the Tibetan Plateau.Appl Phys Res,3(1):
Pan T.,Zhu J.,Hwu W.J.,Jankovic J.2012.The role of alphasynuclein in melanin synthesis in melanoma and dopaminergic neuronal cells.PLoS ONE,7(9):e45183
Rota E.,Tanteri G.,Montori G.,Giachi F.,Delfino G.,Sever D.M.2017.Skin of the red eye tree frog Agalychnis callidryas(Hylidae,Phyllomedusinae)contains lipid glands of the type described in the genus Phyllomedusa.Anat Rec(Hoboken),300(3):503-506
Storz J.F.,Scott G.R.,Cheviron Z.A.2010.Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates.JExp Biol,213(Pt 24):4125-4136
Sun Y.B.,Fu T.T.,Jin J.Q.,Murphy R.W.,Hillis D.M.,Zhang Y.P.,Che J.2018.Species groups distributed across elevational gradients reveal convergent and continuous genetic adaptation to high elevations.Proc Natl Acad Sci U S A,115(45):E10634-E10641
Sun Y.B.,Xiong Z.J.,Xiang X.Y.,Liu S.P.,Zhou W.W.,Tu X.L.,Zhong L.,Wang L.,Wu D.D.,Zhang B.L.,Zhu C.L.,Yang M.M.,Chen H.M.,Li F.,Zhou L.,Feng S.H.,Huang C.,Zhang G.J.,Irwin D.,Hillis D.M.,Murphy R.W.,Yang H.M.,Che J.,Wang J.,Zhang Y.P.2015.Wholegenome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes.Proc Natl Acad Sci U S A,112(11):E1257-E1262
Tattersall G.J.2007.Skin breathing in amphibians.Endothelial Biomedicine:a Comprehensive Reference,85-91
Toledo R.C.,Jared C.1993.The calcified dermal layer in anurans.Comp Biochem Physiol,104(3):443-448
Toledo R.C.,Jared C.1995.Cutaneous granular glands and amphibian venoms.Comp Biochem Physiol,111(1):1-29
Wang G.D.,Zhang B.L.,Zhou W.W.,Li Y.X.,Jin J.Q.,Shao Y.,Yang H.C.,Liu Y.H.,Yan F.,Chen H.M.,Jin L.,Gao F.,Zhang Y.,Li H.,Mao B.,Murphy R.W.,Wake D.B.,Zhang Y.P.,Che J.2018.Selection and environmental adaptation along a path to speciation in the Tibetan frog Nanorana parkeri.Proc Natl Acad Sci U S A,115(22):E5056-E5065
Yang W.Z.,Qi Y.,Bi K.,Fu J.Z.2012.Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species:a comparative transcriptomic analysis of two ranid frogs,Rana chensinensis and R-kukunoris.BMCGenomics,13(1):588
Yang X.,Wang Y.,Zhang Y.,Lee W.H.,Zhang Y.2016.Rich diversity and potency of skin antioxidant peptides revealed a novel molecular basis for high-altitude adaptation of amphibians.Sci Rep,6:19866
Cao Y.,Xie F.,Jiang J.P.2011.Histological observation of skin in fourspecies in the genus Scutiger.Sichun J Zool,30(2):214-2119(In Chinese)
Che J.,Wang K.2016.AmphibiaChina:an online database of Chinese amphibians.Zool Res,37(1):57-59
Che J.,Zhou W.W.,Hu J.S.,Yan F.,Papenfuss T.J.,Wake D.B.,Zhang Y.P.2010.Spiny frogs(Paini)illuminate the history of the Himalayan region and Southeast Asia.Proc Natl Acad Sci U S A,107(31):13765-13770
Cheviron Z.A.,Brumfield R.T.2009.Migration-selection balance and local adaptation of mitochondrial haplotypes in rufouscollared sparrows(Zonotrichia capensis)along an elevational gradient.Evolution,63(6):1593-1605
Cheviron Z.A.,Connaty A.D.,McClelland G.B.,Storz J.F.2014.Functional genomics of adaptation to hypoxic coldstress in high-altitude deer mice:transcriptomic plasticity and thermogenic performance.Evolution,68(1):48-62
Del Bino S.,Bernerd F.2013.Variations in skin colour and the biological consequences of ultraviolet radiation exposure.Br JDermatol,169 Suppl 3:33-40
Delfino G.,Giachi F.,Malentacchi C.,Nosi D.2015.Ultrastructural evidence of serous gland polymorphism in the skin of the Tungara frog Engystomops pustulosus(Anura Leptodactylidae).Anat Rec(Hoboken),298(9):1659-1667
Denver R.J.2009.Stress hormones mediate environment-genotype interactions during amphibian development.Gen Comp Endocrinol,164(1):20-31
Fusco G.,Minelli A.2010.Phenotypic plasticity in development and evolution:facts and concepts.Philos Trans R Soc Lond BBiol Sci,365(1540):547-556
Greenberg N.M.,DeMayo F.,Finegold M.J.,Medina D.,Tilley W.D.,Aspinall J.O.,Cunha G.R.,Donjacour A.A.,Matusik R.J.,Rosen J.M.1995.Prostate cancer in a transgenic mouse.Proc Natl Acad Sci U S A,92(8):3439-3443
Hassanin A.,Ropiquet A.,Couloux A.,Cruaud C.2009.Evolution of the mitochondrial genome in mammals living at high altitude:new insights from a study of the tribe Caprini(Bovidae,Antilopinae).J Mol Evol,68(4):293-310
Huang L.,Li J.,Anboukaria H.,Luo Z.,Zhao M.,Wu H.2016.Comparative transcriptome analyses of seven anurans reveal functions and adaptations of amphibian skin.Sci Rep,6:24069
Jablonski N.G.,Chaplin G.2010.Colloquium paper:human skin pigmentation as an adaptation to UV radiation.Proc Natl Acad Sci U S A,107 Suppl 2:8962-8968
Jia L.L.,Tian C.,Li S.L.2013.Comparative histologial observation of skin in male and female frog(Rana dybouwskii)during breeding season.Chinese Agri Sci Bull,29(2):23-26(In Chinese)
Kim D.S.,Park S.H.,Kwon S.B.,Youn S.W.,Park E.S.,Park K.C.2005.Heat treatment decreases melanin synthesis via protein phosphatase 2A inactivation.Cell Signal,17(8):1023-1031
Liang G.,Wang Q.X.2004.Histological characteristics of the skin and cutaneous glands in Paa quadranus.Chin J Zool,39(4):73-76(In Chinese)
Ma X.Y.,Lu X.2010.Annual cycle of reproductive organs in a Tibetan frog,Nanorana parkeri.Anim Biol,60(3):259-271
Melzer S.,Clerens S.,Bishop P.J.2013.Skin gland morphology and secretory peptides in naturalized Litoria species in New Zealand.J Herpetol,47(4):565-574
Mi Z.P.,Liao W.B.2016.Comparison of skin histostructures in three species of genus Rana.Chin J Zool,51(5):844-852(In Chinese)
Norsang G.,Kocbach L.,Stamnes J.,Tsoja W.2011.Spatial distribution and temporal variation of solar UV radiation over the Tibetan Plateau.Appl Phys Res,3(1):
Pan T.,Zhu J.,Hwu W.J.,Jankovic J.2012.The role of alphasynuclein in melanin synthesis in melanoma and dopaminergic neuronal cells.PLoS ONE,7(9):e45183
Rota E.,Tanteri G.,Montori G.,Giachi F.,Delfino G.,Sever D.M.2017.Skin of the red eye tree frog Agalychnis callidryas(Hylidae,Phyllomedusinae)contains lipid glands of the type described in the genus Phyllomedusa.Anat Rec(Hoboken),300(3):503-506
Storz J.F.,Scott G.R.,Cheviron Z.A.2010.Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates.JExp Biol,213(Pt 24):4125-4136
Sun Y.B.,Fu T.T.,Jin J.Q.,Murphy R.W.,Hillis D.M.,Zhang Y.P.,Che J.2018.Species groups distributed across elevational gradients reveal convergent and continuous genetic adaptation to high elevations.Proc Natl Acad Sci U S A,115(45):E10634-E10641
Sun Y.B.,Xiong Z.J.,Xiang X.Y.,Liu S.P.,Zhou W.W.,Tu X.L.,Zhong L.,Wang L.,Wu D.D.,Zhang B.L.,Zhu C.L.,Yang M.M.,Chen H.M.,Li F.,Zhou L.,Feng S.H.,Huang C.,Zhang G.J.,Irwin D.,Hillis D.M.,Murphy R.W.,Yang H.M.,Che J.,Wang J.,Zhang Y.P.2015.Wholegenome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes.Proc Natl Acad Sci U S A,112(11):E1257-E1262
Tattersall G.J.2007.Skin breathing in amphibians.Endothelial Biomedicine:a Comprehensive Reference,85-91
Toledo R.C.,Jared C.1993.The calcified dermal layer in anurans.Comp Biochem Physiol,104(3):443-448
Toledo R.C.,Jared C.1995.Cutaneous granular glands and amphibian venoms.Comp Biochem Physiol,111(1):1-29
Wang G.D.,Zhang B.L.,Zhou W.W.,Li Y.X.,Jin J.Q.,Shao Y.,Yang H.C.,Liu Y.H.,Yan F.,Chen H.M.,Jin L.,Gao F.,Zhang Y.,Li H.,Mao B.,Murphy R.W.,Wake D.B.,Zhang Y.P.,Che J.2018.Selection and environmental adaptation along a path to speciation in the Tibetan frog Nanorana parkeri.Proc Natl Acad Sci U S A,115(22):E5056-E5065
Yang W.Z.,Qi Y.,Bi K.,Fu J.Z.2012.Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species:a comparative transcriptomic analysis of two ranid frogs,Rana chensinensis and R-kukunoris.BMCGenomics,13(1):588
Yang X.,Wang Y.,Zhang Y.,Lee W.H.,Zhang Y.2016.Rich diversity and potency of skin antioxidant peptides revealed a novel molecular basis for high-altitude adaptation of amphibians.Sci Rep,6:19866