Intra- and interspecific skull variation in two sister species of the subterranean rodent genus Ctenomys (Rodentia, Ctenomyidae): Coupling geometric morphometrics and chromosomal polymorphism

Zoological Journal of the Linnean Society

Volumn 155, Issue 1, 2009, Pages 220-237

  Fernandes, Fabiano Araujo ^a   Fornel, Rodrigo ^a   Cordeiro Estrela, Pedro ^a   Freitas, Thales Renato O ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Chromosomal variability; Phenotypic evolution; Skull morphology

Indexed keywords

CTENOMYIDAE; CTENOMYS; CTENOMYS PEARSONI; CTENOMYS TORQUATUS; RODENTIA;

EID: 58149335345     PISSN: 00244082     EISSN: 10963642     Source Type: Journal    
DOI: 10.1111/j.1096-3642.2008.00428.x     Document Type: Article

References (109)

1. Altuna CA, Francescoli G, Tassino B, Izquierdo I. 1999. Ecoetologia y conservación de mamíferos subterráneos de distribución restringida: El caso de Ctenomys pearsoni (Rodentia, Octodontidae) en el Uruguay. Etología 7 : 47 54.
2. Altuna CA, Lessa EP. 1985. Penial morphology in Uruguayan species of Ctenomys (Rodentia, Octodontidae). Journal of Mammalogy 66 : 483 488.
3. Apfelbaum LI, Massarini AI, Daleffe LE, Reig OA. 1991. Genetic variability in the subterranean rodents Ctenomys australis and Ctenomys porteousi (Rodentia: Octodontidae). Biochemical Systematics and Ecology 19 : 467 476.
4. Avise JC. 2000. Phylogeography: the history and formation of species. Cambridge (MA) : Harvard University Press.
5. Baylac M. 2006. Rmorph: a geometric and multivariate morphometrics library for R. Available from the author.
6. Baylac M, Friess M. 2005. Fourier descriptors, procrustes superimposition and data dimensionality: an example of cranial shape analysis in modern human populations. In : Slice DE, ed. Modern morphometrics in physical anthropology. New York : Springer-Verlag, 145 162.
7. Baylac M, Villemant C, Simbolotti G. 2003. Combining geometric morphometrics with pattern recognition for the investigation of species complexes. Biological Journal of the Linnean Society 80 : 89 98.
8. Berlocher SH. 1998. Origins: a brief history of research on speciation. In : Howard DJ, Berlocher S, eds. Endless forms: species and speciation. Oxford : Oxford University Press, 3 15.
9. Bidau CJ, Giménez MD, Contreras JR. 1996. Especiación cromosómica y la conservacion de la variabilidad genética: El caso del género Ctenomys (Rodentia, Caviomorpha, Ctenomyidae). Mendeliana 12 : 25 37.
10. Bookstein FL. 1991. Morphometric tools for landmark data. Cambridge : Cambridge University Press.
11. Bookstein FL. 1996. Biometrics, biomathematics and the morphometric synthesis. Bulletin of Mathematical Biology 58 : 313 365.
12. Braggio E, Giménez DG, Contreras J, Justo E, Bidau CJ. 1999. Karyotypic variation in populations of Ctenomys (Ctenomyidae) from La Pampa Province (Argentina). Caryologia 52 : 131 140.
13. Bromham L, Woolfit M, Lee MS, Rambaut A. 2002. Testing the relationship between morphological and molecular rates of change along phylogenies. Evolution 56 : 1921 1930.
14. Bush GL. 1975. Modes of animal speciation. Annual Review of Ecology and Systematics 6 : 339 364.
15. Castillo HA, Cortinas MN, Lessa EP. 2005. Rapid diversification of South American tuco-tucos (Ctenomys; Rodentia, Ctenomydae): contrasting mitochondrial and nuclear intron sequences. Journal of Mammalogy 86 : 170 179.
16. Chatti N, Said K, Catalan J, Britton-Davidian J, Auffray JC. 1999. Developmental instability in wild chromosomal hybrids of the house mouse. Evolution 53 : 1268 1279.
17. Cook JA, Anderson S, Yates A. 1990. Notes on Bolivian mammals 6. The genus Ctenomys (Rodentia, Ctenomyidae) in the highlands. American Museum Novitates 2980 : 1 27.
18. Cook JA, Lessa EP. 1998. Are rates of diversification in subterranean South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidea) unusually high? Evolution 52 : 1521 1527.
19. Cordeiro-Estrela P, Baylac M, Denys C, Marinho-Filho J. 2006. Interspecific patterns of skull variation between sympatric Brazilian vesper mice: geometric morphometrics assessment. Journal of Mammalogy 87 : 1270 1279.
20. Corti M, Ciabatti CM, Capanna E. 1990. Parapatric hybridization in the chromosomal speciation of the house mouse. Biological Journal of the Linnean Society 41 : 203 214.
21. Corti M, Fadda C, Simson S, Nevo E. 1996. Size and shape variation in the mandible of the fossorial rodent Spalax ehrenbergi: a procustes analysis of three dimensions. In : Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE, eds. Advances in morphometrics. New York, London : NATO ASI Sciences, Life Sciences, 303 320.
22. Corti M, Rohlf FJ. 2001. Chromosomal speciation and phenotypic evolution in the house mouse. Biological Journal of the Linnean Society 73 : 99 112.
23. D'Anatro A, Lessa EP. 2006. Geometric morphometric analysis of geographic variation in the Rio Negro tuco-tuco, Ctenomys rionegrensis (Rodentia: Ctenomyidae). Mammalian Biology 71 : 288 298.
24. D'Elia G, Lessa EP, Cook JA. 1998. Geographic structure, gene flow, and maintenance of melanism in Ctenomys rionegrensis (Rodentia, Octodontidae). Zeitschrift für Säugetierkunde 63 : 285 296.
25. D'Elia G, Lessa EP, Cook JA. 1999. Molecular phylogeny of tuco-tucos, genus Ctenomys (Rodentia, Octodontidae): evaluation of the mendocinus species group and the evolution of asymmetric sperm. Journal of Mammalian Evolution 6 : 19 38.
26. Dobigny G, Baylac M, Denys C. 2002. Geometric morphometrics, neural networks and diagnosis of sibling Taterillus species (Rodentia, Gerbillinae). Biological Journal of the Linnean Society 77 : 319 327.
27. Dryden IL, Mardia KV. 1998. Statistical shape analysis. New York : John Wiley, Sons, Inc.
28. El Jundi TARJ, Freitas TRO. 2004. Genetic and demographic structure in a population of Ctenomys lami (Rodentia-Ctenomyidae). Hereditas 140 : 18 23.
29. Fernández-Stolz GP, Stolz JFB, Freitas TRO. 2007. Bottlenecks and dispersal in the tuco-tuco-das dunas, Ctenomys flamarioni (Rodentia: Ctenomyidae) in south Brazil. Journal of Mammalogy 88 : 935 945.
30. Freitas TRO, Lessa EP. 1984. Cytogenetics and morphology of Ctenomys torquatus (Rodentia-Octodontidae). Journal of Mammalogy 65 : 637 642.
31. Freitas TRO. 1995. Geographical distribution of sperm forms in the genus Ctenomys. Brazilian Journal of Genetics 18 : 43 46.
32. Freitas TRO. 1997. Chromosome polymorphism in Ctenomys minutus (Rodentia-Octodontidae). Revista Brasileira de Genética 20 : 1 7.
33. Freitas TRO. 2001. Tuco-tucos (Rodentia, Octodontidae) in southern Brazil: Ctenomys lami Spec. Nov. separated from C. minutus Nehring 1887. Studies on Neotropical Fauna and Environment 36 : 1 8.
34. Freitas TRO. 2005. Analysis of skull morphology in 15 species of the genus Ctenomys, including seven karyologically distinct forms of Ctenomys minutus (Rodentia: Ctenomyidae). In : Lacey EA, Myers P, eds. Mammalian diversification: from chromosomes to phylogeography (a celebration of the career of James L. Patton). Vol. 133. Berkeley : University of California Press, 131 156.
35. Freitas TRO. 2006. Cytogenetics status of four Ctenomys species in the South of Brazil. Genetica 126 : 227 235.
36. Freitas TRO. 2007. Ctenomys lami: the highest chromosomal variability in Ctenomys (Rodentia, Ctenomyidae) due to a centric fusion/fission and pericentric inversion system. Acta Theriologica 52 : 171 180.
37. Freygang CC, Marinho JR, Freitas TRO. 2004. New karyotypes and some considerations about the chromosomal diversification of Ctenomys minutus (Rodentia: Ctenomyidae) on the coastal plain of the Brazilian state of Rio Grande do Sul. Genetica 121 : 125 132.
38. Gallardo M. 1991. Karyotypic evolution in Ctenomys (Rodentia, Octodontidae). Journal of Mammalogy 72 : 11 21.
39. Garcia L, Ponsa MM, Egozcue J, Garcia M. 2000a. Cytogenetic variation in Ctenomys perrensis (Rodentia, Ocotodontidae). Biological Journal of the Linnean Society 71 : 615 624.
40. Garcia L, Ponsa MM, Egozcue J, Garcia M. 2000b. Comparative chromosomal analysis and phylogeny in four Ctenomys species (Rodentia, Ocotodontidae). Biological Journal of the Linnean Society 69 : 1 03 120.
41. Gastal MLA. 1994. Density, sexual rate and biometrics data from one population of Ctenomys minutus Nehring, 1887 (Rodentia, Caviomorpha, Ctenomyidae). Iheringia 77 : 25 34.
42. Gava A, Freitas TRO. 2002. Characterization of a hybrid zone between chromosomally divergent populations of Ctenomys minutus (Rodentia; Ctenomyidae). Journal of Mammalogy 83 : 843 851.
43. Gava A, Freitas TRO. 2003. Inter and intraspecific hybridization in tuco-tucos (Ctenomys) from Brazilian coastal plains (Rodentia: Ctenomyidae). Genetica 119 : 11 17.
44. Giménez MD, Contreras JR, Bidau CJ. 1997. Chromosomal variation in Ctenomys pilarensis: a recently described species from eastern Paraguay (Rodentia, Ctenomyidae). Mammalia 61 : 385 398.
45. Giménez MD, Mirol P, Bidau CJ, Searle JB. 2002. Molecular analysis of populations of Ctenomys (Caviomorpha, Rodentia) with high karyotypic variability. Cytogenetics and Genome Research 96 : 130 136.
46. González E. 2001. Guía de Campo de los Mamíferos del Uruguay. Introducción al Estudio de los Mamíferos. Montevideo, Uruguay : Vida Silvestre.
47. Gravilets S, Li H, Vose MD. 1998. Rapid parapatric speciation on holey adaptive landscapes. Proceedings of the Royal Society of London B 265 : 1483 1489.
48. Hanken J, Thorogood P. 1993. Evolution and development of the vertebrate skull: the role of pattern formation. Trends in Ecology and Evolution 8 : 9 15.
49. Harmon LJ, Gibson R. 2006. Multivariate phenotypic evolution among island and mainland populations of the ornate day gecko, Phelsuma ornata. Evolution 60 : 1622 2632.
50. Hood CS. 2000. Geometric morphometric approaches to the study of sexual size dimorphism in mammals. Hystrix 11 : 77 90.
51. Kiblisky P, Brum-Zorrilla N, Perez G, Saez FA. 1977. Variabilidad cromosómica entre diversas poblaciones uruguayas del roedor cavador del género Ctenomys (Rodentia-Octodontidae). Mendeliana 2 : 85 93.
52. King M. 1993. Species evolution. Cambridge : University Press.
53. Klingenberg CP, Badyaev AV, Sowry SM, Beckwith NJ. 2001. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. American Naturalist 157 : 11 23.
54. Lacey E, Patton JL, Cameron GN. 2000. Life underground: the biology of subterranean rodents. Chicago (IL) : University of Chicago Press.
55. Langguth A, Abella A. 1970. Las especies uruguayas del género Ctenomys (Rodentia, Octodontidae). Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo 10 : 1 20.
56. Lessa EP, Cook JA. 1989. Interspecific variation in penial characters in the genus Ctenomys (Rodentia, Octodontidae). Journal of Mammalogy 70 : 856 860.
57. Lessa EP, Langguth A. 1983. Ctenomys pearsoni, n. sp., (Rodentia: Octodontidae), del Uruguay. Resúmenes Comunicaciones Jornadas de Ciencias Naturales del Uruguay 3 : 86 88.
58. Lichtenstein H. 1830 (1827-31). Darstellung neuer order wenig bekannter. Saugethiere in Abbildung und Beschreibungen. Berlin : Luderitz edit.
59. Lucy D, Aykroid R. 2004. GenKern: functions for generating and manipulating kernel density estimates. R package version 1.1-0.
60. Malizia AI, Vassalo AI, Busch C. 1991. Population and habitat characteristics of two sympatric species of Ctenomys (Rodentia: Octodontidae). Acta Theriologica 36 : 87 94.
61. Marinho JR, Freitas TRO. 2000. Intraspecific craniometric variation in a chromosome hibrid zone of Ctenomys minutus (Rodentia, Hystricognathi). Zeitschrift für Säugetierkunde 65 : 226 231.
62. Marinho JR, Freitas TRO. 2006. Population structure of Ctenomys minutus (Rodentia, Ctenomyidae) on the coastal plain of Rio Grande do Sul, Brazil. Acta Theriologica 51 : 53 59.
63. Marroig G, Cheverud JM. 2001. A comparisonof phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World Monkeys. Evolution 55 : 2576 2600.
64. Marroig G, Cheverud JM. 2004. Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? American Naturalist 163 : 417 428.
65. Mascheretti S, Mirol PM, Giménez MD, Bidau CJ, Contreras JR, Searle JB. 2000. Phylogenetics of the speciose and chromosomally variable rodent genus Ctenomys (Ctenomyidae: Octodontoidea), based on mitochondrial cytochrome b sequences. Biological Journal of the Linnean Society 70 : 361 376.
66. Massarini AI, Barros MA, Ortells MO, Reig OA. 1991. Chromosomal polymorphism and small karyotypic differentiation in a group of Ctenomys species from Central Argentina (Rodentia: Octodontidae). Genetica 83 : 131 144.
67. Massarini AI, Barros MA, Ortells MO, Reig OA. 1995. Variabilidad cromosómica en Ctenomys talarum (Rodentia: Octodontidae). Revista Chilena de Historia Natural 68 : 207 214.
68. Massarini AI, Dyzenchauz FJ, Tiranti SI. 1998. Geographic variation of chromosomal polymorphism in nine population of Ctenomys azarae, tuco-tucos of the Ctenomys mendocinus (Rodentia-Octodontidae). Hereditas 128 : 207 211.
69. Massarini AI, Freitas TRO. 2005. Morphological and cytogenetics comparison in species of the mendocinus-group (genus Ctenomys) with emphasis in C. australis and C. flamarioni (Rodentia-Ctenomyidae). Caryologia 58 : 21 27.
70. Monteiro LR, Bordin B, dos Reis SR. 2000. Shape distances, shape spaces and the comparison of morphometric methods. Trends in Ecology and Evolution 15 : 217 220.
71. Mora M, Olivares AI, Vassalo AI. 2003. Size, shape and structural versatility of the skull of the subterranean rodent Ctenomys (Rodentia, Caviomorpha): functional and morphological analysis. Biological Journal of the Linnean Society 78 : 85 96.
72. Moreira DM, Franco MHLP, Freitas TRO, Weimer TA. 1991. Biochemical polymorphisms and phenetic relationships in rodents of the genus Ctenomys from southern Brazil. Biochemical Genetics 29 : 601 615.
73. Nehring A. 1900. Über die Schadel von Ctenomys minutus Nhrg., Ct. torquatus Lich. Und Ct. pundit Nhrg., Sitzungsb Ge. Naturf Fr 9 : 201 210.
74. Nicola PA, Monteriro LR, Pessoa LM, Von Zuben FJ, Rohlf FJ, dos Reis SF. 2003. Congruence of hierarchical localized variation, in cranial shape and molecular phylogenetic structure in spiny rats, genus Trinomys (Rodentia: Echimyidae). Biological Journal of the Linnean Society, London 80 : 385 396.
75. Novello A, Altuna CA. 2002. Cytogenetics and distribution of two new karyomorphs of the Ctenomys pearsoni complex (Rodentia, Octodontidae) from southern Uruguay. Zeitschrift für Säugetierkunde 67 : 188 192.
76. Novello A, Cortinas MN, Suarez M, Musto H. 1996. Cytogenetic and molecular analysis of the satellite DNA of the genus Ctenomys (Rodentia: Octodontidae) from Uruguay. Chromosome Research 4 : 335 339.
77. Novello A, Lessa EP, Sambarino C, Monzón S. 1990. Chromosomal variation in two populations of the genus Ctenomys (Rodentia: Octodontidae) from Uruguay. Zeitschrift für Säugetierkunde 55 : 43 48.
78. Novello A, Lessa EP. 1986. G-Band homology in two karyomorphs of the Ctenomys pearsoni complex (Rodentia: Octodontidae) of Neotropical fossorial rodents. Zeitschrift für Säugetierkunde 51 : 378 380.
79. Novelo A, Villar S. 2006. Chromosome plasticity in Ctenomys (Rodentia, Octodontidae): chromosome 1 evolution and heterochromatin variation. Genetica 127 : 303 309.
80. Ortells MO, Barrantes GE. 1994. A study of genetics distances and variability in several species of the genus Ctenomys (Rodentia, Octodontidae) with special reference to probable causal role of chromosome in speciation. Biological Journal of the Linnean Society 53 : 189 208.
81. Ortells MO, Contreras JR, Reig OA. 1990. New Ctenomys karyotypes (Rodentia, Octodontidae) from north-eastern Argentina and from Paraguay confirm the extreme chromosomal multiformity of the genus. Genetica 82 : 189 291.
82. Ortells MO. 1995. Phylogenetic analysis of G-banded karyotypes among the South American subterranean rodents of the genus Ctenomys (Caviomorpha: Octodontidae), with special reference to chromosomal evolution and speciation. Biological Journal of the Linnean Society 54 : 43 70.
83. Paradis E, Strimmer K, Claude J, Jobb G, Open-Rhein R, Dultheil J, Bolker NB. 2006. APE: analyses of phylogenetic and evolution. R package version 1.8-2.
84. Patton JL, Sherwood SW. 1983. Chromosome evolution and speciation in rodents. Annual Review of Ecology and Systematics 14 : 139 158.
85. Pearson OP. 1959. Biology of the subterranean rodents, Ctenomys, in Peru. Memorians del Museum de Historia Natural 'Javier Prado 9 : 1 56.
86. Reig OA, Busch C, Ortells MO, Contreras JR. 1990. An overview of evolution, systematics, population biology, cytogenetics, molecular biology and speciation in Ctenomys. In : Nevo E, Reig OA, eds. Evolutions of the subterranean mammals at the organismal and molecular levels. New York : Alan R. Liss, Inc, 71 96.
87. Reig OA, Contreras JR, Piantanida MJ. 1966. Contribución a la elucidación de la sistematica de las entidades del genero Ctenomys (Rodentia, Octodontidae). Contribuciones Científicas da Faculdad de Ciencias Exactas y Naturales de la Universidad de Buenos Aires (Zooloía) 6 : 297 352.
88. Reig OA, Kiblisky P. 1969. Chromosome multiformity in the genus Ctenomys (Rodentia: Octodontidae). Chromosoma 28 : 211 244.
89. dos Reis SF. 1990. Mammalian cranial morphometrics: a comparative study of traditional and truss networks. Zoologischer Anzeiger 224 : 225 235.
90. dos Reis SF, Duarte LC, Monteiro LR, Von Zuben FJ. 2002. Geographic variation in cranial morphology in Thrichomys apereoides (Rodentia: Echimyidae). I. Geometric descriptors and patterns of variation in shape. Journal of Mammalogy 83 : 333 344.
91. Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends in Ecology and Evolution 16 : 351 358.
92. Rohlf FJ, Marcus LF. 1993. A revolution in morphometrics. Trends in Ecology and Evolution 8 : 129 132.
93. Rohlf FJ. 1996. Morphometric spaces, shape components and the effects of linear transformations. In : Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE, eds. Advances in morphometrics. NATO ASI Ser. 284 : 117 129.
94. Rohlf FJ. 2000. On the use of shape spaces to compare morphometric methods. Hystrix 11 : 8 24.
95. Rohlf FJ. 2004. TpsUtil, ver. 1.26 software; TpsDig, ver. 1.40 software and TpsREGR, ver. 1.29. Stony Brook : F. James Rohlf. Dept. Ecology and Evolution, State University of New York.
96. Rosi MI, Cona MI, Roig VG. 2002. Current knowledge of the fossorial rodent Ctenomys mendocinus Philippi, 1869 (Rodentia: Ctenomyidae). Mastozoologia Neotropical 9 : 277 296.
97. Saïd K, Auffray JC, Boursot P, Britton-Davidian J. 1999. Is chromosomal speciation occurring in house mice in Tunisia? Biological Journal of the Linnean Society 68 : 387 399.
98. Slamovits CH, Cook JA, Lessa EP, Rossi MS. 2001. Recurrent amplifications and deletions of satellite DNA accompanied chromosomal diversification in South American tuco-tucos (Genus Ctenomys, Rodentia: Octodontidae): a phylogenetic approach. Molecular Biology and Evolution 18 : 1708 1719.
99. Taylor PJ. 2000. Patterns of chromosomal variation in southern African rodents. Journal of Mammalogy 81 : 317 331.
100. Tomasco IH, Lessa EP. 2007. Phylogeography of the tuco-tuco Ctenomys pearsoni: mtDNA variation and its implication for chromosomal differentiation. In : Kelt DA, Lessa EP, Salazar-Bravo J, Patton JL, eds. The quintessential naturalist: honoring the life and legacy of Oliver P. Pearson. Berkeley : University of California Publications in Zoology, 859 882.
101. Vassallo AI. 1998. Functional morphology, comparative behavior, and adaptation in two sympatric subterranean rodents genus Ctenomys (Caviomorpha: Octodontidae). Journal of Zoology, London 244 : 415 427.
102. Venables WN, Ripley BD. 2002. MASS: modern applied statistics with S. New York : Springer.
103. Viegas-Péquignot E, Petit D, Benazzou T, Prod'homme M, Lombard M, Hoffschir F, Descailleaux J, Dutrillaux B. 1986. Phylogénie chromosomique chez les Sciuridae, Gerbillidae et Muridae, et études d'espèces appartenant à d'autres familles de rongeurs. Mammalia 50 : 163 202.
104. Villar S, Martínez-López W, Folle G, Novello A. 2005. Cytogenetic analysis of different Ctenomys (Rodentia, Octodontidae) species from Uruguay using G-banding. Mammalian Biology 70 : 255 260.
105. Voss RS, Marcus LF, Escalante P. 1990. Morphological evolution in muroid rodent. I. Conservative patterns of craniometric covariance and their ontogenetic basis in the neotropical genus Zygodontomys. Evolution 44 : 1568 1587.
106. Wand MP, Jones MC. 1995. Kernel smoothing. London : Chapman, Hall.
107. White MJD. 1978. Modes of speciation. San Francisco : Freeman WH, Co.
108. Wlasiuk G, Garza JC, Lessa EP. 2003. Genetic and geographic differentiation in the Rio Negro tuco-tuco (Ctenomys rionegrensis): inferring the roles of migration and drift from multiple genetic markers. Evolution 57 : 913 926.
109. Ximenes SSF, Fernandes FA, Freitas TRO. 2006. Novos números cariotípicos para espécie Ctenomys torquatus no Rio Grande do Sul. Gramado, Rio Grande do Sul : Anais do I Congresso Sul Americano de Mastozoologia.