Abstract
Squamates exhibit some of the most extreme and fascinating biological adaptations among vertebrates, including the production of a wide diversity of venom toxins. The rapid accumulation of genomic information from squamate reptiles is generating important new context and insights into the biology, the regulation and diversity of venom toxins, and the evolutionary processes that have generated this diversity. It is an exciting time as we discover what the unique aspects of the squamate genome can tell us about the molecular basis of such interesting and diverse phenotypes and explain how the extreme adaptations of squamate biology arose. This chapter reviews what is known about major patterns and evolutionary trends in squamate genomes and discusses how some of these features may relate to the evolution and development of unique features of squamate biology and physiology on the whole, including the evolution and regulation of venom toxins. It also discusses current challenges and obstacles in understanding squamate genome size, diversity, and evolution, and specific issues related to assembling and studying regions of squamate genomes that contain the genes and regulatory regions for venom toxins. Evidence is presented for a relatively constant genome size across squamates even though there have been major shifts in genomic structure and evolutionary processes. Some genomic structural features seem relatively unique to squamates and may have played roles in the evolution of venom toxins.
References
Alfoldi J, Di Palma F, Grabherr M, et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477:587–91.
Bradnam KR, Fass JN, Alexandrov A, Baranay P, Bechner M, Birol I, Boisvert S, Chaptman JA, et al. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. GigaScience. 2013;2:10.
Calvete JJ. Antivenomics and venom phenotyping: a marriage of convenience to address the performance and range of clinical use of antivenoms. Toxicon. 2010;56:1284–91.
Casewell NR, Wuster W, Wagstaff SC, Renjifo C, Richardson MK, Vonk FJ, Harrison RA. The origin and evolution of metalloproteinases in the venom of snakes. Toxicon. 2012;60:119.
Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD. Adaptive evolution and functional redesign of core metabolic proteins in snakes. PLoS One. 2008;3:e2201.
Castoe TA, de Koning APJ, Kim H-M, Gu W, Noonan BP, Naylor G, Jiang ZJ, Parkinson CL, Pollock DD. Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci. 2009a;106:8986–91.
Castoe TA, Gu W, De Koning APJ, Daza JM, Jiang ZJ, Parkinson CL, Pollock DD. Dynamic nucleotide mutation gradients and control region usage in squamate reptile mitochondrial genomes. Cytogenet Genome Res. 2009b;127:112–27.
Castoe T, de Koning A, Hall K, et al. Sequencing the genome of the Burmese python (Python molurus bivittatus) as a model for studying extreme adaptations in snakes. Genome Biol. 2011a;12:1–8.
Castoe TA, Bronikowski AM, Brodie ED, Edwards SV, Pfrender ME, Shapiro MD, Pollock DD, Warren WC. A proposal to sequence the genome of a garter snake (Thamnophis sirtalis). Stand Genomic Sci. 2011b;4:257–70.
Castoe TA, Fox SE, De Koning APJ, Poole AW, Daza JM, Smith EN, Mockler TC, Secor SM, Pollock DD. A multi-organ transcriptome resource for the Burmese python (Python molurus bivittatus). BMC Res Notes. 2011c;4.
Castoe TA, Hall KT, Mboulas MLG, et al. Discovery of highly divergent repeat landscapes in snake genomes using high-throughput sequencing. Genome Biol Evol. 2011d;3:641–53.
Castoe TA, de Koning AP, Hall KT, et al. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci U S A. 2013;110:20645–50.
Crawford NG, Faircloth BC, McCormack JE, Brumfield RT, Winker K, Glenn TC. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol Lett. 2012;8:783–6.
Di-Poi N, Montoya-Burgos JI, Miller H, Pourquie O, Milinkovitch MC, Duboule D. Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature. 2010;464:99–103.
Ezaz T, Quinn A, Miura I, Sarre S, Georges A, Marshall Graves J. The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res. 2005;13:763–76.
Ezaz T, Warre SD, O’Meally D, Marshall Graves JA, Georges A. Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res. 2009;127:249–60.
Fry BG, Vidal N, Norman JA, et al. Early evolution of the venom system in lizards and snakes. Nature. 2006;439:584–8.
Gilbert C, Pace JK, Waters PD. Target site analysis of RTE1_LA and its AfroSINE partner in the elephant genome. Gene. 2008;425:1–8.
Gilbert C, Schaack S, Pace Ii JK, Brindley PJ, Feschotte C. A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature. 2010;464:1347–50.
Gilbert C, Hernandez SS, Flores-Benabib J, Smith EN, Feschotte C. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol Biol Evol. 2012;29:503–15.
Gregory TR. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev. 2001;76:65–101.
Gregory TR. Genome size evolution in animals. In: Gregory TR, editor. The evolution of the genome. Boston: Elsevier Academic Press; 2005. p. 4–71.
Gregory TR. Animal genome size database. 2013. http://www.genomesize.com
Hedges SB, Dudley J, Kumar S. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics. 2006;22:2971–2.
Hedley DW, Friedlander ML, Taylor IW. Application of DNA flow cytometry to paraffin-embedded archival material for the study of aneuploidy and its clinical significance. Cytometry. 1985;6:327–33.
Hillier LW, Miller W, Birney E, et al. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695–716.
Ikeda N, Chijiwa T, Matsubara K, Oda-Ueda N, Hattori S, Matsuda Y, Ohno M. Unique structural characteristics and evolution of a cluster of venom phospholipase A(2) isozyme genes of Protobothrops flavoviridis snake. Gene. 2010;461:15–25.
Janes DE, Organ CL, Edward SV. Variability in sex-determining mechanisms influences genome complexity in Reptilia. Cytogenet Genome Res. 2009;127:242–8.
Janes DE, Chapus C, Gondo Y, Clayton DF, Sinha S, Blatti CA, Organ CL, Fujita MK, Balakrishnan CN, Edward SV. Reptiles and mammals have differentially retained long conserved noncoding sequences from the Amniote ancester. Genome Biol Evol. 2010a;3:102–13.
Janes DE, Organ CL, Fujita MK, Shedlock AM, Edwards SV. Genome evolution in Reptilia, the sister group of mammals. Annu Rev Genomics Hum Genet. 2010b;11(11):239–64.
Jiang ZJ, Castoe TA, Austin CC, Burbrink FT, Herron MD, McGuire JA, Parkinson CL, Pollock DD. Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region. BMC Evol Biol. 2007;7:123.
Kordis D. Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet Genome Res. 2009;127:94–111.
Kordis D, Gubensek F. Bov-B long interspersed repeated DNA (LINE) sequences are present in Vipera ammodytes phospholipase A(2) genes and in genomes of Viperidae snakes. Eur J Biochem. 1997;246:772–9.
Kordis D, Gubensek F. Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. Proc Natl Acad Sci U S A. 1998;95:10704–9.
Kordiš D, Gubenšek F. Molecular evolution of Bov-B LINEs in vertebrates. Gene. 1999;238:171–8.
Kumazawa Y, Ota H, Nishida M, Ozawa T. Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol Biol Evol. 1996;13:1242–54.
Leutwiler LS, Hough-Evans BR, Meyerowitz EM. The DNA of Arabidopsis thaliana. Mol Gen Genet MGG. 1984;194:15–23.
Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, Matsuda Y. Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci. 2006;103:18190–5.
McCormack JE, Faircloth BC, Crawford NG, Gowaty PA, Brumfield RT, Glenn TC. Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis. Genome Res. 2012;22:746–54.
Novick PA, Basta H, Floumanhaft M, McClure MA, Boissinot S. The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. Mol Biol Evol. 2009;26:1811–22.
Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM. The mode and tempo of genome size evolution in eukaryotes. Genome Res. 2007;17:594–601.
Olmo E. Rate of chromosome changes and speciation in reptiles. Genetica. 2005;125:185–203.
Olmo E, Signorino GG. Chromorep: a reptile chromosomes database. http://chromoprep.univpm.it/ (2013).
Organ CL, Moreno RG, Edwards SV. Three tiers of genome evolution in reptiles. Integr Comp Biol. 2008;48:494–504.
Pace JK, Gilbert C, Clark MS, Feschotte C. Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proc Natl Acad Sci. 2008;105:17023–8.
Piskurek O, Okada N. Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals. Proc Natl Acad Sci U S A. 2007;104:12046–51.
Piskurek O, Nishihara H, Okada N. The evolution of two partner LINE/SINE families and a full-length chromodomain-containing Ty3/Gypsy LTR element in the first reptilian genome of Anolis carolinensis. Gene. 2009;441:111–8.
Rodionov AV. Micro versus macro: a review of structure and functions of avian micro- and macrochromosomes. Russ J Genet. 1996;32:597–608.
Rodionov AV, Myakoshina YA, Chelysheva LA, Solovei IV, Gaginskaya ER. Chiasmata on lampbrush chromosomes of Gallus gallus domesticus: a cytogenetic study of recombination frequency and linkage group lengths. Russ J Genet. 1992;28:53–63.
Shedlock AM, Botka CW, Zhao SY, Shetty J, Zhang TT, Liu JS, Deschavanne PJ, Edward SV. Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genorne. Proc Natl Acad Sci U S A. 2007;104:2767–72.
Siigur E, Aaspõllu A, Siigur J. Sequence diversity of Vipera lebetina snake venom gland serine proteinase homologs – result of alternative-splicing or genome alteration. Gene. 2001;263:199–203.
Smith J, Bruley CK, Paton IR, et al. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet. 2000;31:96–103.
Srikulnath K, Nishida C, Matsubara K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y. Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the Japanese four-striped rat snake (Elaphe quadrivirgata, Colubridae, Serpentes). Chromosome Res. 2009;17:975–86.
Vonk FJ, Casewell NR, Henkel CV, et al. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A. 2013;110:20651–6.
Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL. Widespread horizontal transfer of retrotransposons. Proc Natl Acad Sci. 2013;110:1012–6.
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Shaney, K.J. et al. (2014). Squamate Reptile Genomics and Evolution. In: Gopalakrishnakone, P., Calvete, J. (eds) Toxinology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6649-5_34-2
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DOI: https://doi.org/10.1007/978-94-007-6649-5_34-2
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