Modularity as a source of new morphological variation in the mandible of hybrid mice

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Renaud, Sabrina ^a   Alibert, Paul ^b   Auffray, Jean Christophe ^c  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Geometric morphometrics; House mouse; Hybridization; Mandible shape; Mus musculus; Transgressive phenotypes

Indexed keywords

DIVERGENCE; DOMINANCE; HYBRID; HYBRIDIZATION; MORPHOLOGY; MORPHOMETRY; PHENOTYPE; RODENT;

MUS; MUS MUSCULUS;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; HISTOLOGY; HYBRIDIZATION; MANDIBLE; MOUSE;

ANIMALS; BODY SIZE; HYBRIDIZATION, GENETIC; MANDIBLE; MICE; MODELS, BIOLOGICAL;

EID: 84864555872     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-141     Document Type: Article

References (65)

1. Morphological innovation and developmental genetics. Marshall CR, Orr HA, Patel NH, Proc Natl Acad Sci USA 1999 96 9995 9996 10.1073/pnas.96.18.9995 10468549
2. Linking develoment with generation of novelty in mammalian teeth. Jernvall J, Proc Natl Acad Sci USA 2000 97 6 2641 2645 10.1073/pnas.050586297 10706636
3. Evolution of novelty in the cichlid dentition. Streelman JT, Albertson RC, J Exp Zool (Mol Dev Evol) 2006 306B 216 226 10.1002/jez.b.21101
4. Complete congruence between morphological and rbcL-based phylogenies in birches and related species (Betulaceae). Bousquet J, Strauss SH, Li P, Mol Biol Evol 1992 9 6 1076 1088 1435235
5. Correlated rates of molecular and morphological evolution. Omland KE, Evolution 1997 51 5 1381 1393 10.2307/2411190
6. On morphological clocks and paleophylogeography: towards a timescale forSorexhybrid zones. Polly PD, Genetica 2001 112-113 339 357 18038183
7. Paleophylogeography ofSorex araneus: molar shape as a morphological marker for fossil shrews. Polly PD, Mammalia 2003 68 2 233 243
8. Schluter D, The ecology of adaptive radiation Oxford: Oxford University Press 2000
9. Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents. Renaud S, Chevret P, Michaux J, Zoologica Scripta 2007 36 525 535 10.1111/j.1463-6409.2007.00297.x
10. Genetic and morphometric evidence of introgression between two species of moles (Insectivora:Talpa europaeaandTalpa romana) in central Italy. Loy A, Capula M, Palombi A, Capanna E, J Zool London 2001 254 229 238 10.1017/S0952836901000747
11. Relative warp analysis of skull shape across the hybrid zone of the house mouse (Mus musculus) in Denmark. Auffray J-C, Alibert P, Latieule C, Dod B, J Zool London 1996 240 441 455 10.1111/j.1469-7998.1996.tb05297.x
12. Morphological variation in intergrade pupfish populations from the Pecos River, Texas, U.S.A. Wilde GR, Echelle AA, J Fish Biol 1997 50 523 539 10.1111/j.1095-8649.1997.tb01947.x
13. Hybridisation between two cyprinid fishes in a novel habitat: genetics, morphology and life-history traits. Hayden B, Pulcini D, Kelly-Quinn M, O'Grady M, Caffrey J, McGrath A, Mariani S, BMC Evolutionary Biology 2010 10 169 10.1186/1471-2148-10-169 20529364
14. Elliptic Fourier analysis of the form of genitalia in twoSpodopteraspecies and their hybrids (Lepidoptera: Noctuidae). Monti L, Baylac M, Lalanne-Cassou B, Biol J Linn Soc 2001 72 391 400 10.1111/j.1095-8312.2001. tb01325.x
15. Shape based assignments tests suggest transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae). Nolte AW, Sheets HD, Front Zool 2005 2 11 10.1186/1742-9994-2-11 15987531
16. Geometric morphometrics reveals body shape differences between sympatric redfishSebastes mentella,Sebastes fasciatusand their hybrids in the Gulf of St Lawrence. Valentin A, Sévigny J-M, Chanut J-P, J Fish Biol 2002 60 857 875
17. Hybridization promotes evolvability in African cichlids: connections between transgressive segregation and phenotypic integration. Parsons KJ, Son YH, Albertson RC, Evol Biol 2011 38 3 306 315 10.1007/s11692-011-9126-7
18. An invasive lineage of sculpins,Cottussp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Nolte AW, Freyhof J, Stemshorn KC, Tautz D, Proc Roy Soc Lond Biol Sci (serie B) 2005 272 2379 2387 10.1098/rspb.2005.3231
19. Genetic distance between species predicts novel trait expression in their hybrids. Stelkens R, Seehausen O, Evolution 2009 63 4 884 897 10.1111/j.1558-5646.2008.00599.x 19220450
20. Hybrid speciation. Mallet J, Nature 2007 446 15 279 283 17361174
21. Natural hybridization generates mammalian lineage with species characteristics. Larsen PA, Marchán-Rivadeneira MR, Baker RJ, Proc Natl Acad Sci USA 2010 107 25 11447 11452 10.1073/pnas.1000133107 20534512
22. Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Klingenberg CP, Leamy LJ, Routman EJ, Cheverud JM, Genetics 2001 157 785 802 11156997
23. Analysis of quantitative trait locus effects on the size and shape of mandibular molars in mice. Workman MS, Leamy LJ, Routman EJ, Cheverud JM, Genetics 2002 160 1573 1586 11973311
24. A comparative assessment of mandible shape in a consomic strain panel of the house mouse (Mus musculus)-implications for epistasis and evolvability of quantitative traits. Boell L, Gregorova S, Forejt J, Tautz D, BMC Evol Biol 2011 11 309 10.1186/1471-2148-11-309 22011306
25. Integration and modularity of quantitative trait locus effefts on geometric shape in the mouse mandible. Klingenberg CP, Leamy LJ, Cheverud JM, Genetics 2004 166 1909 1921 10.1534/genetics.166.4.1909 15126408
26. Evolution and development of shape: integrating quantitative approaches. Klingenberg CP, Nat Rev Genet 2010 11 623 635 20697423
27. Evolutionary modularity of the mouse mandible: dissecting the effect of chromosomal reorganizations and isolation by distance in a Robertsonian system ofMus musculus domesticus. Munoz-Munoz F, Sans-Fuetes MA, Lopez-Fuster MJ, Ventura J, J Evol Biol 2011 24 1763 1776 10.1111/j.1420-9101.2011.02312.x 21615588
28. A model for development and evolution of complex morphological structures. Atchley WR, Hall BK, Biol Rev 1991 66 2 101 157 10.1111/j.1469-185X. 1991.tb01138.x 1863686
29. Development of the mouse mandible: a model system for complexmorphological structures. Klingenberg CP, Navarro N, Evolution of the House Mouse Cambridge: Cambridge University Press, Macholán M, Baird SJE, Munclinger P, Piálek J, 2012 135 149
30. Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Klingenberg CP, Mebus K, Auffray J-C, Evol Dev 2003 5 5 522 531 10.1046/j.1525-142X.2003.03057.x 12950630
31. Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Monteiro LR, Bonato V, Reis SF, Evol Dev 2005 7 5 429 439 10.1111/j.1525-142X.2005.05047.x 16174036
32. The evolution of house mice. Boursot P, Auffray J-C, Britton-Davidian J, Bonhomme F, Annu Rev Ecol Systemat 1993 24 119 152 10.1146/annurev.es.24.110193. 001003
33. House mice as models in systematic biology. Sage RD, Atchley WR, Capanna E, Syst Biol 1993 42 4 523 561 10.1093/sysbio/42.4.523
34. Fluctuating asymmetry in theMus musculushybrid zone: a heterotic effect in disrupted co-adapted genomes. Alibert P, Renaud S, Dod B, Bonhomme F, Auffray J-C, Proc Roy Soc Lond B 1994 258 53 59 10.1098/rspb.1994.0141
35. Inferences of selection and migration in the Danish house mouse hybrid zone. Raufaste N, Orth A, Belkhir K, Senet D, Smalda C, Baird SJE, Bonhomme F, Dod B, Boursot P, Biol J Linn Soc 2005 84 593 616 10.1111/j.1095-8312.2005. 00457.x
36. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Macholán M, Munclinger P, ugerková M, Dufková P, Bímová B, Boíková E, Zima J, Piálek J, Evolution 2007 61 4 746 771 10.1111/j.1558-5646.2007.00065.x 17439609
37. Mandible shape in hybrid mice. Renaud S, Alibert P, Auffray J-C, Naturwissenschaften 2009 96 1043 1050 10.1007/s00114-009-0563-4 19504055
38. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Rieseberg LH, Widmer A, Arntz AM, Burke JM, Phil Trans R Soc Lond B 2003 358 1141 1147 10.1098/rstb.2003.1283
39. Hybridization and adaptive radiation. Seehausen O, Trends Ecol Evol 2004 19 4 198 207 10.1016/j.tree.2004.01.003 16701254
40. Genetic architecture sets limits on transgressive segregation in hybrid cyclid fishes. Albertson RC, Kocher TD, Evolution 2005 59 3 686 690 15856710
41. Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Bell MA, Travis MP, Trends Ecol Evol 2005 20 7 358 361 10.1016/j.tree.2005.04.021 16701394
42. Morphometric studies in inbred and hybrid House mice (Mussp.): Multivariate analysis of size and shape. Thorpe RS, Leamy L, J Zool Lond 1983 199 421 432
43. Developmental stability, fitness, and trait size in laboratory hybrids between European subspecies of the house mouse. Alibert P, Fel-Clair F, Manolakou K, Britton-Davidian J, Auffray J-C, Evolution 1997 51 4 1284 1295 10.2307/2411057
44. Morphological evolution in the mandible of spiny rats, genusTrinomys(Rodentia: Echimyidae). Monteiro LR, Reis SF, J Zool Systemat Evol Res 2005 43 4 332 338 10.1111/j.1439-0469.2005.00323.x
45. TPSdig2. Rohlf FJ, Ecology and Evolution Stony Brook: SUNY 2010
46. TPSRelw. Rohlf FJ, Ecology and Evolution Stony Brook: SUNY 2010
47. Extensions of the Procrustes method for the optimal superimposition of landmarks. Rohlf FJ, Slice D, Syst Zool 1990 39 40 59 10.2307/2992207
48. Bookstein F, Morphometric tools for landmark data: geometry and biology New York: Cambridge University Press 1991
49. TPSsmall. Rohlf FJ, Ecology and Evolution Stony Brook: SUNY 2003
50. The conceptual and statistical relationship between modularity and morphological integration. Mitteroecker P, Bookstein F, Syst Biol 2007 56 5 818 836 10.1080/10635150701648029 17934997
51. Le traitement des variables vectorielles. Escoufier Y, Biometrics 1973 29 751 760 10.2307/2529140
52. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Klingenberg CP, Evol Dev 2009 11 4 405 421 10.1111/j.1525-142X.2009.00347.x 19601974
53. The ade4 package: implementing the duality diagram for ecologists. Dray S, Dufour A-B, J Stat Software 2007 22 1 20
54. Use of two-block partial least-squares to study covariation in shape. Rohlf FJ, Corti M, Syst Biol 2000 49 740 753 10.1080/106351500750049806 12116437
55. Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Renaud S, Auffray J-C, Michaux J, Evolution 2006 60 8 1701 1717 17017070
56. Comparative functional morphology of mandibular forward movement during mastication of two murid rodents,Apodemus speciosus(Murinae) andClethrionomys rufocanus(Arvicolinae). Satoh K, J Morphol 1997 231 131 142 10.1002/(SICI)1097- 4687(199702)231:2<131::AID-JMOR2>3.0.CO;2-H 8989873
57. Do precocial mammals develop at a faster rate? A comparison of rates of skull development inSigmodon fulviventerandMus musculus domesticus. Zelditch ML, Lundrigan BL, Sheets HD, Garland TJ, J Evol Biol 2003 16 708 720 10.1046/j.1420-9101.2003.00568.x 14632234
58. Effect of different masticatory functional and mechanical demands on the structural adaptation of the mandibular alveolar bone in young growing rats. Mavropoulos A, Kiliardis S, Bresin A, Ammann P, Bone 2004 35 191 197 10.1016/j.bone.2004.03.020 15207756
59. Adaptation and plasticity in insular evolution of the house mouse mandible. Renaud S, Auffray J-C, J Zool Systemat Evol Res 2010 48 2 138 150 10.1111/j.1439-0469.2009.00527.x
60. Plasticity of mandibular biomineralization in myostatin-deficient mice. Ravosa MJ, Klopp EB, Pinchoff J, Stock SR, Hamrick MW, J Morphol 2007 268 275 282 10.1002/jmor.10517 17299778
61. Epigenetic effects on the mouse mandible: common features and discrepancies in remodeling due to muscular dystrophy and response to food consistency. Renaud S, Auffray J-C, de La Porte S, BMC Evol Biol 2010 20 18
62. Modularity of the rodent mandible: integrating bones, muscles, and teeth. Zelditch ML, Wood AR, Bonett RM, Swiderski DL, Evol Dev 2008 10 6 756 766 10.1111/j.1525-142X.2008.00290.x 19021747
63. The developmental basis of variational modularity: insights from quantitative genetics, morphometrics, and developmental biology. Mitteroecker P, Evol Biol 2009 36 377 385 10.1007/s11692-009-9075-6
64. Hybridization as an invasion of the genome. Mallet J, Trends Ecol Evol 2005 20 229 237 10.1016/j.tree.2005.02.010 16701374
65. A draft sequence of the neandertal genome. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH-Y, et al. Science 2010 328 710 722 10.1126/science.1188021 20448178