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http://dx.doi.org/10.5808/GI.2015.13.4.102

Role of Chromosome Changes in Crocodylus Evolution and Diversity  

Srikulnath, Kornsorn (Laboratory of Animal Cytogenetics and Comparative Genomics, Department of Genetics, Faculty of Science, Kasetsart University)
Thapana, Watcharaporn (Laboratory of Animal Cytogenetics and Comparative Genomics, Department of Genetics, Faculty of Science, Kasetsart University)
Muangmai, Narongrit (Department of Fishery Biology, Faculty of Fisheries, Kasetsart University)
Publication Information
Genomics & Informatics / v.13, no.4, 2015 , pp. 102-111 More about this Journal
Abstract
The karyotypes of most species of crocodilians were studied using conventional and molecular cytogenetics. These provided an important contribution of chromosomal rearrangements for the evolutionary processes of Crocodylia and Sauropsida (birds and reptiles). The karyotypic features of crocodilians contain small diploid chromosome numbers (30~42), with little interspecific variation of the chromosome arm number (fundamental number) among crocodiles (56~60). This suggested that centric fusion and/or fission events occurred in the lineage, leading to crocodilian evolution and diversity. The chromosome numbers of Alligator, Caiman, Melanosuchus, Paleosuchus, Gavialis, Tomistoma, Mecistops, and Osteolaemus were stable within each genus, whereas those of Crocodylus (crocodylians) varied within the taxa. This agreed with molecular phylogeny that suggested a highly recent radiation of Crocodylus species. Karyotype analysis also suggests the direction of molecular phylogenetic placement among Crocodylus species and their migration from the Indo-Pacific to Africa and The New World. Crocodylus species originated from an ancestor in the Indo-Pacific around 9~16 million years ago (MYA) in the mid-Miocene, with a rapid radiation and dispersion into Africa 8~12 MYA. This was followed by a trans-Atlantic dispersion to the New World between 4~8 MYA in the Pliocene. The chromosomes provided a better understanding of crocodilian evolution and diversity, which will be useful for further study of the genome evolution in Crocodylia.
Keywords
centric fusion/fission; crocodile; evolution; fundamental number; karyotype;
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  • Reference
1 Brochu CA. Phylogenetic approaches toward crocodylian history. Annu Rev Earth Planet Sci 2003;31:357-397.   DOI
2 Uetz P, Hosek J. The Reptile Database. Peter Ietz, 2015. Accessed 2015 Oct 19. Available from: http://www.reptile-database.org.
3 Gatesy J, Amato G, Norell M, DeSalle R, Hayashi C. Combined support for wholesale taxic atavism in gavialine crocodylians. Syst Biol 2003;52:403-422.   DOI
4 Gatesy J, Amato G. The rapid accumulation of consistent molecular support for intergeneric crocodylian relationships. Mol Phylogenet Evol 2008;48:1232-1237.   DOI
5 Harshman J, Huddleston CJ, Bollback JP, Parsons TJ, Braun MJ. True and false gharials: a nuclear gene phylogeny of Crocodylia. Syst Biol 2003;52:386-402.   DOI
6 Schmitz A, Mansfeld P, Hekkala E, Shine T, Nickel H, Amato G, et al. Molecular evidence for species level divergence in African Nile crocodiles Crocodylus niloticus (Laurenti, 1786). C R Palevol 2003;2:703-712.   DOI
7 Janke A, Gullberg A, Hughes S, Aggarwal RK, Arnason U. Mitogenomic analyses place the gharial (Gavialis gangeticus) on the crocodile tree and provide pre-K/T divergence times for most crocodilians. J Mol Evol 2005;61:620-626.   DOI
8 McAliley LR, Willis RE, Ray DA, White PS, Brochu CA, Densmore LD III. Are crocodiles really monophyletic? Evidence for subdivisions from sequence and morphological data. Mol Phylogenet Evol 2006;39:16-32.   DOI
9 Li Y, Wu X, Ji X, Yan P, Amato G. The complete mitochondrial genome of salt-water crocodile (Crocodylus porosus) and phylogeny of crocodilians. J Genet Genomics 2007;34:119-128.   DOI
10 Willis RE. Transthyretin gene (TTR) intron 1 elucidates crocodylian phylogenetic relationships. Mol Phylogenet Evol 2009;53:1049-1054.   DOI
11 Feng G, Wu X, Yan P, Li X. Two complete mitochondrial genomes of Crocodylus and implications for crocodilians phylogeny. Amphibia-Reptilia 2010;31:299-309.   DOI
12 Meganathan PR, Dubey B, Batzer MA, Ray DA, Haque I. Molecular phylogenetic analyses of genus Crocodylus (Eusuchia, Crocodylia, Crocodylidae) and the taxonomic position of Crocodylus porosus. Mol Phylogenet Evol 2010;57:393-402.   DOI
13 Meganathan PR, Dubey B, Batzer MA, Ray DA, Haque I. Complete mitochondrial genome sequences of three Crocodylus species and their comparison within the Order Crocodylia. Gene 2011;478:35-41.   DOI
14 Man Z, Yishu W, Peng Y, Xiaobing W. Crocodilian phylogeny inferred from twelve mitochondrial protein-coding genes, with new complete mitochondrial genomic sequences for Crocodylus acutus and Crocodylus novaeguineae. Mol Phylogenet Evol 2011;60:62-67.   DOI
15 Meredith RW, Hekkala ER, Amato G, Gatesy J. A phylogenetic hypothesis for Crocodylus (Crocodylia) based on mitochondrial DNA: evidence for a trans-Atlantic voyage from Africa to the New World. Mol Phylogenet Evol 2011;60:183-191.   DOI
16 Oaks JR. A time-calibrated species tree of Crocodylia reveals a recent radiation of the true crocodiles. Evolution 2011;65: 3285-3297.   DOI
17 Olmo E, Signorino GG. CHROMOREP: a reptile chromosomes database. Chromorep, 2015. Accessed 2015 Feb 16. Available from: http://chromorep.univpm.it/.
18 Srikulnath K, Thongpan A, Suputtitada S, Apisitwanich S. New haplotype of the complete mitochondrial genome of Crocodylus siamensis and its species-specific DNA markers: distinguishing C. siamensis from C. porosus in Thailand. Mol Biol Rep 2012;39:4709-4717.   DOI
19 Muller J, Reisz RR. Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. Bioessays 2005;27:1069-1075.   DOI
20 Cohen MM, Gans C. The chromosomes of the order Crocodilia. Cytogenetics 1970;9:81-105.   DOI
21 Kawagoshi T, Nishida C, Ota H, Kumazawa Y, Endo H, Matsuda Y. Molecular structures of centromeric heterochromatin and karyotypic evolution in the Siamese crocodile (Crocodylus siamensis) (Crocodylidae, Crocodylia). Chromosome Res 2008;16:1119-1132.   DOI
22 Srikulnath K, Thongpan A, Apisitwanich S. Karyotypes of Siamese crocodile (Crocodylus siamensis) and saltwater crocodile (Crocodylus porosus) using Het- and G-banding. In: 15th National Genetic Conference, 2007 May 23-25, Songkhla, Thailand.
23 Kasai F, O'Brien PC, Martin S, Ferguson-Smith MA. Extensive homology of chicken macrochromosomes in the karyotypes of Trachemys scripta elegans and Crocodylus niloticus revealed by chromosome painting despite long divergence times. Cytogenet Genome Res 2012;136:303-307.   DOI
24 Ji X, Wu X, Yan P, Amato G. Complete sequence and gene organization of the mitochondrial genome of siamensis crocodile (Crocodylus siamensis). Mol Biol Rep 2008;35:133-138.   DOI
25 Nakatani Y, Takeda H, Kohara Y, Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 2007;17:1254-1265.   DOI
26 Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K, Isobe T, et al. Highly conserved linkage homology between birds and turtles: bird and turtle chromosomes are precise counterparts of each other. Chromosome Res 2005;13:601-615.   DOI
27 Uno Y, Nishida C, Tarui H, Ishishita S, Takagi C, Nishimura O, et al. Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS One 2012;7:e53027.   DOI
28 Lang JW, Andrews HV. Temperature-dependent sex determination in crocodilians. J Exp Zool 1994;270:28-44.   DOI
29 Ellegren H. Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol 2010;25:283-291.   DOI
30 Olmo E. Rate of chromosome changes and speciation in reptiles. Genetica 2005;125:185-203.   DOI
31 Demuth J. Do sex chromosomes affect speciation rate? (Retrospective on DOI 10.1002/bies.201100164). Bioessays 2014;36:632.   DOI
32 International Chicken Genome Sequencing Consortium. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004;432:695-716.   DOI
33 Alfoldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 2011;477:587-591.   DOI
34 Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, et al. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 2014;346:1254449.   DOI
35 Castoe TA, de Koning AP, Hall KT, Card DC, Schield DR, Fujita MK, et al. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci USA 2013;110:20645-20650.   DOI
36 Wan QH, Pan SK, Hu L, Zhu Y, Xu PW, Xia JQ, et al. Genome analysis and signature discovery for diving and sensory properties of the endangered Chinese alligator. Cell Res 2013;23:1091-1105.   DOI
37 Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ, McCleary RJ, et al. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci USA 2013;110:20651-20656.   DOI
38 Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, et al. Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci USA 2006;103:18190-18195.   DOI
39 Matsubara K, Kuraku S, Tarui H, Nishimura O, Nishida C, Agata K, et al. Intra-genomic GC heterogeneity in sauropsids: evolutionary insights from cDNA mapping and GC(3) profiling in snake. BMC Genomics 2012;13:604.   DOI
40 Srikulnath K, Nishida C, Matsubara K, Uno Y, Thongpan A, Suputtitada S, et al. 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;17:975-986.   DOI
41 Young MJ, O'Meally D, Sarre SD, Georges A, Ezaz T. Molecular cytogenetic map of the central bearded dragon, Pogona vitticeps (Squamata: Agamidae). Chromosome Res 2013;21:361-374.   DOI
42 Srikulnath K, Uno Y, Nishida C, Matsuda Y. Karyotype evolution in monitor lizards: cross-species chromosome mapping of cDNA reveals highly conserved synteny and gene order in the Toxicofera clade. Chromosome Res 2013;21:805-819.   DOI
43 Srikulnath K, Matsubara K, Uno Y, Nishida C, Olsson M, Matsuda Y. Identification of the linkage group of the Z sex chromosomes of the sand lizard (Lacerta agilis, Lacertidae) and elucidation of karyotype evolution in lacertid lizards. Chromosoma 2014;123:563-575.   DOI
44 Srikulnath K, Uno Y, Nishida C, Ota H, Matsuda Y. Karyotype reorganization in the Hokou Gecko (Gekko hokouensis, Gekkonidae): the process of microchromosome disappearance in Gekkota. PLoS One 2015;10:e0134829.   DOI
45 Matzke MA, Varga F, Berger H, Schernthaner J, Schweizer D, Mayr B, et al. A 41-42 bp tandemly repeated sequence isolated from nuclear envelopes of chicken erythrocytes is located predominantly on microchromosomes. Chromosoma 1990;99:131-137.   DOI
46 Matzke AJ, Varga F, Gruendler P, Unfried I, Berger H, Mayr B, et al. Characterization of a new repetitive sequence that is enriched on microchromosomes of turkey. Chromosoma 1992;102:9-14.   DOI
47 Tanaka K, Suzuki T, Nojiri T, Yamagata T, Namikawa T, Matsuda Y. Characterization and chromosomal distribution of a novel satellite DNA sequence of Japanese quail (Coturnix coturnix japonica). J Hered 2000;91:412-415.   DOI
48 Yamada K, Nishida-Umehara C, Matsuda Y. Molecular and cytogenetic characterization of site-specific repetitive DNA sequences in the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae). Chromosome Res 2005;13:33-46.   DOI
49 Yamada K, Shibusawa M, Tsudzuki M, Matsuda Y. Molecular cloning and characterization of novel centromeric repetitive DNA sequences in the blue-breasted quail (Coturnix chinensis, Galliformes). Cytogenet Genome Res 2002;98:255-261.   DOI
50 Yamada K, Nishida-Umehara C, Matsuda Y. Characterization and chromosomal distribution of novel satellite DNA sequences of the lesser rhea (Pterocnemia pennata) and the greater rhea (Rhea americana). Chromosome Res 2002;10:513-523.   DOI
51 Chaiprasertsri N, Uno Y, Peyachoknagul S, Prakhongcheep O, Baicharoen S, Charernsuk S, et al. Highly species-specific centromeric repetitive DNA sequences in lizards: molecular cytogenetic characterization of a novel family of satellite DNA sequences isolated from the water monitor lizard (Varanus salvator macromaculatus, Platynota). J Hered 2013;104:798-806.   DOI
52 Matsubara K, Uno Y, Srikulnath K, Seki R, Nishida C, Matsuda Y. Molecular cloning and characterization of satellite DNA sequences from constitutive heterochromatin of the habu snake (Protobothrops flavoviridis, Viperidae) and the Burmese python (Python bivittatus, Pythonidae). Chromosoma 2015;124:529-539.   DOI
53 Norell MA. The higher level relationships of the extant Crocodylia. J Herpetol 1989;23:325-335.   DOI
54 Poe S. Data set incongruence and the phylogeny of crocodilians. Syst Biol 1996;45:393-414.   DOI
55 Tchernov E. Evolution of the Crocodiles in East and North Africa. Paris: Editions du Centre National de la Recherche Scientifique, 1986.
56 Piras P, Colangelo P, Adams DC, Buscalioni A, Cubo J, Kotsakis T, et al. The Gavialis-Tomistoma debate: the contribution of skull ontogenetic allometry and growth trajectories to the study of crocodylian relationships. Evol Dev 2010;12:568-579.   DOI
57 Suh A, Churakov G, Ramakodi MP, Platt RN II, Jurka J, Kojima KK, et al. Multiple lineages of ancient CR1 retroposons shaped the early genome evolution of amniotes. Genome Biol Evol 2015;7:205-217.   DOI
58 Brochu CA. Phylogenetic relationships and divergence timing of Crocodylus based on morphology and the fossil record. Copeia 2000;2000:657-673.   DOI
59 Aoki R. Fossil crocodilians from the late tertiary strata in the Sinda Basin, eastern Zaire. Afr Stud Monogr 1992;17:67-85.
60 Pickford M. Late Cenozoic crocodiles (Reptilia:Crocodylidae) from the Western Rift, Uganda. In: Geology and Paleobiology of the Albertine Rift Valley, Uganda-Zaire. Vol. 2. Paleobiology/Paleobiologie (Senut B, Pickford M, eds.). Orleans: Centre International pour la Formation et les Echanges Geologiques, 1994. pp. 137-155.
61 Fitzsimmons NN, Buchan JC, Lam PV, Polet G, Hung TT, Thang NQ, et al. Identification of purebred Crocodylus siamensis for reintroduction in Vietnam. J Exp Zool 2002;294:373-381.   DOI
62 Miller KG, Fairbanks RG, Mountain GS. Tertiary oxygen isotope synthesis, sea level history, and continental margin erosion. Paleoceanography 1987;2:1-19.   DOI
63 Salazar-Bravo J, Dragoo JW, Tinnin DS, Yates TL. Phylogeny and evolution of the neotropical rodent genus Calomys: inferences from mitochondrial DNA sequence data. Mol Phylogenet Evol 2001;20:173-184.   DOI
64 Taplin L, Grigg GC. Historical zoogeography of the eusuchian crocodilians: a physiological perspective. Am Zool 1989;29:885-901.   DOI
65 Markwick PJ. Crocodilian diversity in space and time: the role of climate in paleoecology and its implication for understanding K/T extinctions. Paleobiology 1998;24:470-497.   DOI
66 Ross JP. Crocodiles: Status Survey and Conservation Action Plan. 2nd ed. IUCN/SSC Crocodile Specialist Group. Gland: IUCN, 1998.
67 Colangelo P, Corti M, Verheyen E, Annesi F, Oguge N, Makundi RH, et al. Mitochondrial phylogeny reveals differential modes of chromosomal evolution in the genus Tatera (Rodentia: Gerbillinae) in Africa. Mol Phylogenet Evol 2005;35:556-568.   DOI
68 Ramos R, de Buffrenil V, Ross JP. Current status of the Cuban Crocodile, C. rhombifer, in the wild. In: Proceedings of the 12th Working Meeting of the IUCN-SSC Crocodile Specialist Group. Gland: IUCN, 1994. pp. 113-140.
69 Ray DA, Dever JA, Platt SG, Rainwater TR, Finger AG, McMurry ST, et al. Low levels of nucleotide diversity in Crocodylus moreletii and evidence of hybridization with C. acutus. Conserv Genet 2004;5:449-462.   DOI
70 Chavananikul V, Wattanodorn S, Youngprapakorn P. Karyotypes of 5 species of crocodile kept in Samutprakan Crocodile Farm and Zoo. In: The 12th Working Meeting of the IUCN-SSC Crocodile Specialist Group. Gland: IUCN, 1994. pp. 58-62.
71 Sill WD. The zoogeography of the Crocodilia. Copeia 1968;1968:76-88.   DOI
72 Delfino M, Rook L. African crocodylians in the Late Neogene of Europe: a revision of Crocodylus bambolii Ristori, 1890. J Paleontol 2008;82:336-343.   DOI
73 Brooks DR, O'Grady RT. Crocodilians and their helminth parasites: macroevolutionary considerations. Am Zool 1989;29:873-883.   DOI
74 Brochu CA, Njau J, Blumenschine RJ, Densmore LD. A new horned crocodile from the Plio-Pleistocene hominid sites at Olduvai Gorge, Tanzania. PLoS One 2010;5:e9333.   DOI
75 Griffin DL. Aridity and humidity: two aspects of the late Miocene climate of North Africa and the Mediterranean. Palaeogeogr Palaeoclimatol Palaeoecol 2002;182:65-91.   DOI
76 Delfino M, Bohme M, Rook L. First European evidence for transcontinental dispersal of Crocodylus (late Neogene of southern Italy). Zool J Linn Soc 2007;149:293-307.   DOI
77 Ford D, Golonka J. Phanerozoic paleogeography, paleoenvironment, and lithofacies maps of the circum-Atlantic margins. Mar Pet Geol 2003;20:249-285.   DOI
78 de Queiroz A. The resurrection of oceanic dispersal in historical biogeography. Trends Ecol Evol 2005;20:68-73.   DOI