Adaptive Evolution of the Hox Gene Family for Development in Bats and Dolphins

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Liang, Lu ^a,c   Shen, Yong Yi ^a,b   Pan, Xiao Wei ^d   Zhou, Tai Cheng ^d   Yang, Chao ^d   Irwin, David M ^a,e,f   Zhang, Ya Ping ^a,d  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b XIAMEN UNIVERSITY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d YUNNAN UNIVERSITY   (China)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BAT; DEVELOPMENTAL STAGE; DOLPHIN; EMBRYO DEVELOPMENT; FORELIMB; GENE AMPLIFICATION; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CONSERVATION; HOX GENE; MOLECULAR EVOLUTION; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PANCREAS; PHYLOGENETIC TREE; PHYLOGENY; SEQUENCE ALIGNMENT; THYMUS; UNINDEXED SEQUENCE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; METABOLISM; PHYSIOLOGY;

CETACEA; MAMMALIA; MYOTIS DAVIDII; MYOTIS LUCIFUGUS; PHOCOENIDAE; PTEROPUS ALECTO; PTEROPUS VAMPYRUS; TURSIOPS TRUNCATUS;

ANIMALS; CHIROPTERA; DOLPHINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX;

EID: 84879340459     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065944     Document Type: Article

References (60)

1. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, et al. (2011) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334: 521-524.
2. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, et al. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580-584.
3. Shen YY, Liang L, Zhu ZH, Zhou WP, Irwin DM, et al. (2010) Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proceedings Of the National Academy of Sciences, USA 107: 8666-8671.
4. Kunz TH, Fenton MB (2003) Bat Ecology. Chicago: Chicago University Press.
5. Adams RA, (1992) Stages of development and sequence of bone formation in the little brown bat, Myotis lucifugus. Journal of Mammalogy 73: 160-167.
6. Brigham RM, Ianuzzo CD, Hamilton N, Fenton MB, (1990) Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis lucifugus). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 160: 183-186.
7. Powers LV, Kandarian SC, Kunz TH, (1991) Ontogeny of flight in the little brown bat, Myotis lucifugus: behavior, morphology, and muscle histochemistry. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 168: 675-685.
8. Schutt WA Jr, Cobb MA, Petrie JL, Hermanson JW, (1994) Ontogeny of the pectoralis muscle in the little brown bat, Myotis lucifugus. Journal Of Morphology 220: 295-305.
9. Adams RA, Pedersen SC (2000) Ontogeny, functional ecology, and evolution of bats: Cambridge University Press.
10. Maina JN, King AS, (1984) Correlations between structure and function in the design of the bat lung: a morphometric study. Journal Of Experimental Biology 111: 43-61.
11. Fordyce RE, Barnes LG, (1994) The evolutionary history of whales and dolphins. Annual Review Of Earth And Planetary Sciences 22: 419-455.
12. Cooper LN, Berta A, Dawson SD, Reidenberg JS, (2007) Evolution of hyperphalangy and digit reduction in the cetacean manus. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 290: 654-672.
13. Vaughan TA, Ryan JM, Czaplewski NJ (2010) Mammalogy. Sudbury, Massachusetts: Jones and Bartlett Press.
14. Berta A, Sumich JL, Kovacs KM (2006) Marine Mammals: Evolutionary Biology. San Diego: Academic Press.
15. Kanwisher J, Sundnes G (1966) Thermal regulation in cetaceans. Berkeley: University of California Press.
16. Pearson JC, Lemons D, McGinnis W, (2005) Modulating Hox gene functions during animal body patterning. Nature Reviews Genetics 6: 893-904.
17. Wellik DM, (2007) Hox patterning of the vertebrate axial skeleton. Developmental Dynamics 236: 2454-2463.
18. Di-Poi N, Montoya-Burgos JI, Miller H, Pourquie O, Milinkovitch MC, et al. (2010) Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 464: 99-103.
19. McGinnis W, (1992) Homeobox genes and axial patterning. Cell 68: 283-302.
20. Duboule D, Dolle P, (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. The EMBO Journal 8: 1497-1505.
21. Kmita M, Duboule D, (2003) Organizing axes in time and space; 25 years of colinear tinkering. Science 301: 331-333.
22. Iimura T, Pourquié O, (2007) Hox genes in time and space during vertebrate body formation. Development, growth & differentiation 49: 265-275.
23. Wyngaarden LA, Hopyan S, (2008) Plasticity of proximal-distal cell fate in the mammalian limb bud. Developmental Biology 313: 225-233.
24. Zákány J, Kmita M, Duboule D, (2004) A dual role for Hox genes in limb anterior-posterior asymmetry. Science 304: 1669-1672.
25. Stelnicki EJ, Kömüves LG, Kwong AO, Holmes D, Klein P, et al. (1998) HOX homeobox genes exhibit spatial and temporal changes in expression during human skin development. The Journal of investigative dermatology 110: 110-115.
26. Godwin AR, Capecchi MR, (1998) Hoxc13 mutant mice lack external hair. Genes & Development 12: 11-20.
27. Mori M, Nakagami H, Rodriguez-Araujo G, Nimura K, Kaneda Y, (2012) Essential role for miR-196a in brown adipogenesis of white fat progenitor cells. PLoS Biology 10: e1001314.
28. Favier B, Dollé P, (1997) Developmental functions of mammalian Hox genes. Molecular human reproduction 3: 115-131.
29. Di Bonito M, Narita Y, Avallone B, Sequino L, Mancuso M, et al. (2013) Assembly of the Auditory Circuitry by a Hox Genetic Network in the Mouse Brainstem. PLoS genetics 9: e1003249.
30. Sordino P, Van Der Hoeven F, Duboule D, (1995) Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375: 678-681.
31. Goodman FR, (2002) Limb malformations and the human Hox genes. American Journal Of Medical Genetics 112: 256-265.
32. van Scherpenzeel TV, Remacle S, Picard J, Cornu G, Gofflot F, et al. (2005) Mutation analysis of the HOX paralogous 4-13 genes in children with acute lymphoid malignancies: Identification of a novel germline mutation of HOXD4 leading to a partial loss-of-function. Human Mutation 25: 384-395.
33. Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, et al. (2013) Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339: 456-460.
34. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
36. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology And Evolution 24: 1586-1591.
37. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, et al. (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614-618.
38. Murphy WJ, Eizirik E, O'Brien SJ, Madsen O, Scally M, et al. (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348-2351.
39. Zhang J, Nielsen R, Yang Z, (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology And Evolution 22: 2472-2479.
40. Akaike H, (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723.
41. Posada D, Buckley TR, (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793-808.
42. Darriba D, Taboada GL, Doallo R, Posada D, (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
43. Stamatakis A, Hoover P, Rougemont J, (2008) A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57: 758-771.
44. Thewissen JGM, Babcock SK, (1992) The origin of flight in bats. Bioscience 42: 340-345.
45. Teeling EC, Scally M, Kao DJ, Romagnoli ML, Springer MS, et al. (2000) Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403: 188-192.
46. Wang Z, Yuan L, Rossiter SJ, Zuo X, Ru B, et al. (2009) Adaptive evolution of 5′ HoxD genes in the origin and diversification of the cetacean flipper. Molecular Biology And Evolution 26: 613-622.
47. Taghon T, Stolz F, De Smedt M, Cnockaert M, Verhasselt B, et al. (2002) HOX-A10 regulates hematopoietic lineage commitment: evidence for a monocyte-specific transcription factor. Blood 99: 1197-1204.
48. Yueh YG, Gardner DP, Kappen C, (1998) Evidence for regulation of cartilage differentiation by the homeobox gene Hoxc-8. Proceedings Of the National Academy of Sciences, USA 95: 9956-9961.
49. Zákány J, Duboule D, (1999) Hox genes in digit development and evolution. Cell And Tissue Research 296: 19-25.
50. Jones FS, Holst BD, Minowa O, De Robertis EM, Edelman GM, (1993) Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3). Proceedings Of the National Academy of Sciences, USA 90: 6557-6561.
51. Geisen MJ, Di Meglio T, Pasqualetti M, Ducret S, Brunet JF, et al. (2008) Hox paralog group 2 genes control the migration of mouse pontine neurons through slit-robo signaling. PLoS Biology 6: e142.
52. Segara D, Biankin AV, Kench JG, Langusch CC, Dawson AC, et al. (2005) Expression of HOXB2, a retinoic acid signaling target in pancreatic cancer and pancreatic intraepithelial neoplasia. Clinical Cancer Research 11: 3587-3596.
53. Davenne M, Maconochie MK, Neun R, Pattyn A, Chambon P, et al. (1999) Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22: 677-691.
54. Chen F, Capecchi MR, (1997) Targeted mutations in hoxa-9 and hoxb-9 reveal synergistic interactions. Developmental Biology 181: 186-196.
55. DeLynn R, Lovewell G, Wells RS, Early G, (2011) Congenital Scoliosis of a Bottlenose Dolphin. Journal of wildlife diseases 47: 979-983.
56. Xu B, Wellik DM, (2011) Axial Hox9 activity establishes the posterior field in the developing forelimb. Proceedings Of the National Academy of Sciences, USA 108: 4888-4891.
57. Chen CH, Cretekos CJ, Rasweiler JJ IV, Behringer RR, (2005) Hoxd13 expression in the developing limbs of the short-tailed fruit bat, Carollia perspicillata. Evolution & Development 7: 130-141.
58. Chew KY, Yu H, Pask AJ, Shaw G, Renfree MB, (2012) HOXA13 and HOXD13 expression during development of the syndactylous digits in the marsupial Macropus eugenii. BMC Developmental Biology 12: 2.
59. Cretekos CJ, Deng JM, Green ED, Rasweiler JJ, Behringer RR, (2007) Isolation, genomic structure and developmental expression of Fgf8 in the short-tailed fruit bat, Carollia perspicillata. Integrative Journal of Developmental Biology 51: 333-338.
60. Hockman D, Cretekos CJ, Mason MK, Behringer RR, Jacobs DS, et al. (2008) A second wave of Sonic hedgehog expression during the development of the bat limb. Proceedings of the National Academy of Sciences, USA 105: 16982-16987.