[1].Evolution of Phenotype and Mitochondrial Genome Reveals Limbless and Body-elongated Squamates may Change Their Energy Basis for Locomotion[J].Asian Herpetological Research,2021,12(2):213-220.[doi:10.16373/j.cnki.ahr.200134]
 Zeng WANG,Wei WU,Jinlong REN,et al.Evolution of Phenotype and Mitochondrial Genome Reveals Limbless and Body-elongated Squamates may Change Their Energy Basis for Locomotion[J].Asian Herpetological Research(AHR),2021,12(2):213-220.[doi:10.16373/j.cnki.ahr.200134]

Evolution of Phenotype and Mitochondrial Genome Reveals Limbless and Body-elongated Squamates may Change Their Energy Basis for Locomotion()

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]



Evolution of Phenotype and Mitochondrial Genome Reveals Limbless and Body-elongated Squamates may Change Their Energy Basis for Locomotion
Zeng WANG12 Wei WU12 Jinlong REN12 Changjun PENG1 Dechun JIANG1 Jiatang LI134*
1 CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, Sichuan, China
2 University of Chinese Academy of Sciences, Beijing 100049, China
3 Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin Nay Pyi Taw 05282, Myanmar
4 CAS Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, Yunan, China
limb-reduction mitogenome morphology selective pressure Squamata
Limb reduction in Squamata present the dramatic characteristic to focus and usually accompanied with particularly morphological modifications, impacting tremendous locomotion changing and might generate different energy requirement. Herein, we combined both morphological and mitochondrial genomic data to explore the evolution of phenotypic transformation and mitochondrial genome of limbless and body-elongated squamates. We collected phenotypic measurements of 503 individuals, representing limbed or limbless taxa across all major lineages in Squamata to investigate the morphological correlations with limb-reduction. Furthermore, we provided the mitochondrial genome of the representative limbless and elongated species Dibamus bourreti (Angel, 1935) to detect selective constraints on limbless clades with published mitogenomes of other squamate reptiles. Our results evidenced that body elongation had certain negative relationship with limb-reduction in Squamata lineage and Lacertilia lineage (R = –0.495, P < 2.2e-16; R= –0.332, P = 1.1e-13, respectively), while tail length showed slight correlation in both clades (R = 0.156, P = 4.3e-04; R= 0.192, P = 2.1e-05, respectively). Besides, detection demonstrated that ATP6 has experienced accelerated evolution among limbless lineages, suggesting selective pressure on mitogenomes may play an essential role in energy disparity for locomotion of limbed and limbless squamates.


Arnold S. J. 1983. Morphology, performance and fitness. Am Zool, 23(2): 347–361
Bejder L., Hall B. K. 2002. Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss. Evol Dev, 4(6): 445–458
Bergmann J. P., Morinaga G. 2019. The convergent evolution of snake-like forms by divergent evolutionary pathways in squamate reptiles. Evolution, 73(3): 481–496
Bergmann P. J., Irschick D. J. 2010. Alternate pathways of body shape evolution translate into common patterns of locomotor evolution in two clades of lizards. Evolution, 64(6): 1569–1582
Bergmann P. J., Morinaga G., Freitas E. S., Irschick D. J., Wagner G. P., Siler C. D. 2020. Locomotion and palaeoclimate explain the re-evolution of quadrupedal body form in Brachymeles lizards. Proc Biol Sci, 287(1938): 20201994
Bernt M., Donath A., Juhling F., Externbrink F., Florentz C., Fritzsch G., Putz J., Middendorf M., Stadler P. F. 2013. MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol, 69(2): 313–319
Bonett R. M., Blair A. L. 2017. Evidence for complex life cycle constraints on salamander body form diversification. Proc Natl Acad Sci U S A, 114(37): 9936–9941
Boore J. L. 1999. Animal mitochondrial genomes. Nucleic Acids Res, 27(8): 1767–1780
Brandley M. C., Huelsenbeck J. P., Wiens J. J. 2008. Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution, 62(8): 2042–2064
Buchholtz E. A., Booth A. C., Webbink K. E. 2007. Vertebral anatomy in the Florida manatee, Trichechus manatus latirostris: a developmental and evolutionary analysis. Anat Rec, 290(6): 624-637
Buchholtz E. A., Schur S. A. 2004. Vertebral osteology in Delphinidae (Cetacea). Zool J Linn Soc, 140(3): 383–401
Calsbeek R. 2008. An ecological twist on themorphology–performance–fitness axis. Evol Ecol Res, 10(2): 197–212
Caputo V., Guarino F. M., Angelini F. 2000. Body elongation and placentome evolution in the scincid lizard genus Chalcides (Squamata, Scincidae). Ital J Zool, 67(4): 385–391
Carroll R. L. 1997. The fossil record of elongation and limb reduction as a model of evolutionary patterns. J Morphol, 232: 241
Castellana S., Vicario S., Saccone C. 2011. Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein coding genes. Genome Biol Evol, 3: 1067–1079
Chen M. L., Liu J. L., Chen D. L., Guo X. G. 2019. The complete mitochondrial genome of a blue-tailed skink (Plestiodon tunganus) endemic to Sichuan Basin. Mitochondrial DNA B, 4(1): 1109–1110
Das J. 2006. The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays, 28(9): 890–901
Dierckxsens N., Mardulyn P., Smits G. 2017. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res, 45(4): e18
Fontanillas P., D?Praz A., Giorgi M. S., Perrin N. 2005. Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white-toothed shrew, Crocidura russula. Mol Ecol, 14(2): 661–670
Futuyma D. J. 2005. Evolution. Sunderland, MA: Sinauer Associates
Galis F., Arntzen J. W., Lande R. 2010. Dollo’s law and the irreversibility of digit loss in Bachia. Evolution, 64(8): 2466–2476
Gans C. 1962. Terrestrial locomotion without limbs. Am Zool, 2: 167–182
Gans C. 1975. Tetrapod limlessness: evolution and functional corollaries. Am Zool, 15: 455-467
Gans C. 1986. Locomotion of limbless vertebrates: pattern and evolution. Herpetologica, 42: 33–46
Gans C., Fusari M. 1994. Locomotor analysis of surface propulsion by three species of reduced-limbed fossorial lizards (Lerista: Scincidae) from western Australia. J Morphol, 222(3): 309–326
Gans C., Gasc J. P. 1990. Tests on the locomotion of the elongate and limbless reptile Ophisaurus apodus (Sauria: Anguidae). J Zool, 220(4): 517–536
Garland J. T., Losos J. B. 1994. Ecological morphology of locomotor performance in squamate reptiles. In: P C Wainwright and S Reilly (eds.) Ecological Morphology: Integrative Organismal Biology. University of Chicago Press, Chicago, 240–302
Greer A. E. 1985. The relationships of the Lizard Genera Anelytropsis and Dibamus. J Herpetol, 19(1): 116–156
Grizante M. B., Brandt R., Kohlsdorf T. 2012. Evolution of body elongation in gymnophthalmid lizards: Relationships with climate. PLoS ONE, 7(11): e49772
Jacobsen M. W., Pujolar J. M., Hansen M. M. 2015. Relationship between amino acid changes in mitochondrial ATP6 and life-history variation in anguillid eels. Biol Lett, 11(3): 20150014
Jiang D. C., Klaus S., Zhang Y. P., Hillis M. D., Li J. T. 2019. Asymmetric biotic interchange across the Bering land bridge between Eurasia and North America, Natl Sci Rev, 6(4): 739–745
Kucharczyk R., Ezkurdia N., Couplan E., Procaccio V., Ackerman S. H., Blondel M., di Rago J.-P. 2010. Consequences of the pathogenic T9176C mutation of human mitochondrial DNA on yeast mitochondrial ATP synthase. Biochim Biophys Acta Bioenerg, 1797(6): 1105–1112
Lande R. 1978. Evolutionary mechanisms of limb loss in tetrapods. Evolution, 32: 73–92
Law C. J., Slater G. J., Mehta R. S. 2019. Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs. Evolution, 73(4): 735–749
Lee M. S. Y., Skinner A., Camacho A., Patten M. 2013. The relationship between limb reduction, body elongation and geographical range in lizards (Lerista, Scincidae). J Biogeogr, 40(7): 1290–1297
Lowe T. M., Chan P. P. 2016. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res, 44(W1): 54–57
Mehta R. S., Ward A. B., Alfaro M. E., Wainwright P. C. 2010. Elongation of the body in eels. Integr Comp Biol, 50(6): 1091–1105
Meiklejohn C. D., Montooth K. L., Rand D. M. 2007. Positive and negative selection on the mitochondrial genome. Trends Genet, 23(6): 259–263
Miralles A., Hipsley C. A., Erens J., Gehara M., Rakotoarison A., Glaw F., Muller J., Vences M. 2015. Distinct patterns of desynchronized limb regression in malagasy scincine lizards (Squamata, Scincidae). PLoS ONE, 10(6): e0126074
Mitterboeck T. F., Adamowicz S. J. 2013. Flight loss linked to faster molecular evolution in insects. Proc Biol Sci, 280(1767): 20131128
Mitterboeck T. F., Liu S., Adamowicz S. J., Fu J., Zhang R., Song W., Meusemann K., Zhou X. 2017. Positive and relaxed selection associated with flight evolution and loss in insect transcriptomes. Gigascience, 6(10): 1–14
Morinaga G., Bergmann J. P. 2017. Convergent body shapes have evolved via deterministic and historically contingent pathways in Lerista lizards. Biol J Linn Soc, 121(4): 858–875
Morinaga G., Bergmann P. J. 2019. Angles and waves: intervertebral joint angles and axial kinematics of limbed lizards, limbless lizards, and snakes. Zoology, 134: 16–26
Morinaga G., Bergmann P. J. 2020. Evolution of fossorial locomotion in the transition from tetrapod to snake-like in lizards. Proc Biol Sci, 287(1923): 20200192
Parra-Olea G., Wake D. B. 2001. Extreme morphological and ecological homoplasy in tropical salamanders. Proc Natl Acad Sci U S A, 98(14): 7888-7891
Pyron R. A., Burbrink F. T., Wiens J. J. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol, 13(1): 93
Quah E. S. H., Sah S. A. M., Grismer L. L., Grassby-Lewis R. 2017. A new species of Dibamus Duméril & Bibron 1839 (Squamata: Dibamidae) from a hill station in Peninsular Malaysia. Raffles B Zool, 65: 681–690
R core team. 2020 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
Ren J. L., Wang K., Jiang K., Guo P., Li J. T. 2017. A new species of the Southeast Asian genus Opisthotropis (Serpentes: Colubridae: Natricinae) from western Hunan, China. Zool Res, 38(5): 251–263
Renous S., Hofling E., Gasc J. P. 1998. Respective role of the axialand appendicular systems in relation to the transition to limblessness. Acta Biotheor, 46: 141–156
Saraste M. 1999. Oxidative phosphorylation at the fin de siècle. Science, 283(5407): 1488–1493
Shen Y. Y., Liang L., Zhu Z. H., Zhou W. P., Irwin D. M., Zhang Y. P. 2010. Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proc Natl Acad Sci U S A, 107(19): 8666–8671
Shen Y. Y., Shi P., Sun Y. B., Zhang Y. P. 2009. Relaxation of selective constraints on avian mitochondrial DNA following the degeneration of flight ability. Genome Res, 19(10): 1760–1765
Siler C. D., Fuiten A. M., Jones R. M., Alcala A. C., Brown R. M. 2011. Phylogeny-based species delimitation in philippine slender skinks (Reptilia: Squamata: Scincidae) II: Taxonomic revision of Brachymeles samarensis and description of five new species. Herpetol Monogr, 25(1): 76–112
Soares P., Abrantes D., Rito T., Thomson N., Radivojac P., Li B., Macaulay V., Samuels D. C., Pereira L. 2013. uating purifying selection in the mitochondrial DNA of various mammalian species. PLoS ONE, 8(3): e58993
Sperl W., Jesina P., Zeman J., Mayr J. A., Demeirleir L., VanCoster R., Pickova A., Hansikova H., Houst’kova H., Krejcik Z., Koch J., Smet J., Muss W., Holme E., Houstek J. 2006. Deficiency of mitochondrial ATP synthase of nuclear genetic origin. Neuromuscular Disord, 16(12): 821–829
Stewart J. B., Freyer C., Elson J. L., Wredenberg A., Cansu Z., Trifunovic A., Larsson N. G. 2008. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol, 6(1): e10
Sun Y. B., Shen Y. Y., Irwin D. M., Zhang Y. P. 2011. uating the roles of energetic functional constraints on teleost mitochondrial-encoded protein evolution. Mol Biol Evol, 28(1): 39–44
Townsend T., Larson A., Louis E., Macey J. R. 2004. Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Syst Biol, 53(5): 735–757
Townsend T. M., Leavitt D. H., Reeder T. W. 2011. Intercontinental dispersal by a microendemic burrowing reptile (Dibamidae). Proc Biol Sci, 278(1718): 2568–2574
Uetz P., Freed P., Ho?ek J. 2020. The reptile database. The reptile database. Retrieved from http:// www.reptile-database.org. Accessed 17 Dec 2020
Urosevic A., Slijepcevic M. D., Arntzen J. W., Ivanovic A. 2016. Vertebral shape and body elongation in Triturus newts. Zoology, 119(5): 439-446
Webb P. W. 1982. Locomotor Patterns in the evolution of actinopterygian fishes. Am Zool, 22: 329–342
Wiens J. J., Brandley M. C., Reeder T. W. 2006. Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution, 60: 123–141
Wiens J. J., Slingluff J. L. 2001. How lizards turn into snakes: a phylogenetic analysis of body form evolution in anguid lizards. Evolution, 55: 2303–2318
Woltering J. M. 2012. From lizard to snake; behind the evolution of an extreme body plan. Curr Genomics, 13(4): 289–299
Yang Z. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci, 13(5), 555–556
Young R. L., Haselkorn T. S., Badyaev A. V. 2007. Functional equivalence of morphologies enables morphological and ecological diversity. Evolution, 61(11): 2480–2492
Yu Z. P., Seim I., Yin M. X., Tian R., Sun D., Ren W. H., Yang G., Xu S. X. 2021. Comparative analyses of aging-related genes in long-lived mammals provide insights into natural longevity. The Innovation, 2(2): 100108
Zhang B., Zhang Y. H., Wang X., Zhang H. X., Lin Q. 2017. The mitochondrial genome of a sea anemone Bolocera sp. exhibits novel genetic structures potentially involved in adaptation to the deep-sea environment. Evol Dev, 7(13): 4951–4962
Zhao E., Zhao K., Zhou K. 1999. Fauna Sinica: Reptilia. Vol. 2. Squamata, Lacertilia. Beijing, China: Science Press, 1–403 (In Chinese)
Zheng Y., Wiens J. J. 2016. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol, 94(Pt B): 537–547

更新日期/Last Update: 2021-06-25