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Mandible shape in hybrid mice

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Abstract

Hybridisation between closely related species is frequently seen as retarding evolutionary divergence and can also promote it by creating novel phenotypes due to new genetic combinations and developmental interactions. We therefore investigated how hybridisation affects the shape of the mouse mandible, a well-known feature in evo–devo studies. Parental groups corresponded to two strains of the European mouse sub-species Mus musculus domesticus and Mus musculus musculus. Parents and hybrids were bred in controlled conditions. The mandibles of F1 hybrids are mostly intermediate between parental phenotypes as expected for a complex multigenic character. Nevertheless, a transgressive effect as well as an increased phenotypic variance characterise the hybrids. This suggests that hybridisation between the two subspecies could lead to a higher phenotypic variance due to complex interactions among the parental genomes including non-additive genetic effects. The major direction of variance is conserved, however, among hybrids and parent groups. Hybridisation may thus play a role in the production of original transgressive phenotypes occurring following pre-existing patterns of variance.

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References

  • Albertson RC, Kocher TD (2005) Genetic architecture sets limits on transgressive segregation in hybrid cyclid fishes. Evolution 59:686–690

    Article  PubMed  Google Scholar 

  • Albertson RC, Streelman JT, Kocher TD (2003) Directional selection has shaped the oral jaws of Lake Malawi cichlids fishes. Proc Natl Acad Sci USA 100:5252–5257

    Article  PubMed  CAS  Google Scholar 

  • Albertson RC, Streelman JT, Kocher TD, Yelick PC (2005) Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proc Natl Acad Sci USA 102:16287–16292

    Article  PubMed  CAS  Google Scholar 

  • Alibert P, Renaud S, Dod B, Bonhomme F, Auffray J-C (1994) Fluctuating asymmetry in the Mus musculus hybrid zone: a heterotic effect in disrupted co-adapted genomes. Proc R Soc Lond B 258:53–59

    Article  CAS  Google Scholar 

  • Alibert P, Fel-Clair F, Manolakou K, Britton-Davidian J, Auffray J-C (1997) Developmental stability, fitness, and trait size in laboratory hybrids between European subspecies of the house mouse. Evolution 51(4):1284–1295

    Article  Google Scholar 

  • Auffray J-C, Alibert P, Latieule C, Dod B (1996a) Relative warp analysis of skull shape across the hybrid zone of the house mouse (Mus musculus) in Denmark. J Zool Lond 240:441–455

    Article  Google Scholar 

  • Auffray J-C, Alibert P, Renaud S, Orth A, Bonhomme F (1996b) Fluctuating asymmetry in Mus musculus subspecific hybridization. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE (eds) Advances in morphometrics. Plenum, New York, pp 275–283

    Google Scholar 

  • Bell MA, Travis MP (2005) Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends Ecol Evol 20:358–361

    Article  PubMed  Google Scholar 

  • Boursot P, Auffray J-C, Britton-Davidian J, Bonhomme F (1993) The evolution of house mice. Annu Rev Ecol Syst 24:119–152

    Article  Google Scholar 

  • Cardini A, Elton S (2007) Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology 126:121–134

    Article  Google Scholar 

  • Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561

    Article  Google Scholar 

  • Debat V, Alibert P, David P, Paradis E, Auffray J-C (2000) Independence between developmental stability and canalization in the skull of the house mouse. Proc R Soc Lond B 267:423–430

    Article  CAS  Google Scholar 

  • Dod B, Jermiin LS, Boursot P, Chapman VH, Nielsen JT, Bonhomme F (1993) Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J Evol Biol 6(4):529–546

    Article  Google Scholar 

  • Klingenberg CP (1996) Multivariate allometry. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE (eds) Advances in morphometrics. Plenum, New York, pp 23–49

    Google Scholar 

  • Klingenberg CP, Mebus K, Auffray J-C (2003) Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evol Dev 5:522–531

    Article  PubMed  Google Scholar 

  • Klingenberg CP, Leamy LJ, Cheverud JM (2004) Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166:1909–1921

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg CP, Leamy LJ, Routman EJ, Cheverud JM (2001) Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Genetics 157:785–802

    PubMed  CAS  Google Scholar 

  • Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comput Graph Image Process 18:259–278

    Article  Google Scholar 

  • Lomolino MV (1985) Body size of mammals on islands: the island rule reexamined. Am Nat 125:310–316

    Article  Google Scholar 

  • Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699

    Article  Google Scholar 

  • Loy A, Capula M, Palombi A, Capanna E (2001) Genetic and morphometric evidence of introgression between two species of moles (Insectivora: Talpa europaea and Talpa romana) in Central Italy. J Zool Lond 254:229–238

    Article  Google Scholar 

  • Michaux J, Chevret P, Renaud S (2007) Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation. J Zool Syst Evol Res 45:263–279

    Article  Google Scholar 

  • Monteiro LR, Bonato V, SFd R (2005) Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evol Dev 7:429–439

    Article  PubMed  Google Scholar 

  • Monti L, Baylac M, Lalanne-Cassou B (2001) Elliptic Fourier analysis of the form of genitalia in two Spodoptera species and their hybrids (Lepidoptera: Noctuidae). Biol J Linn Soc 72:391–400

    Article  Google Scholar 

  • Moulia C, Aussel JP, Bonhomme F, Boursot P, Nielsen JT, Renaud F (1991) Wormy mice in a hybrid zone: A genetic control of susceptibility to parasite infection. J Evol Biol 4(4):679–687

    Article  Google Scholar 

  • Nolte AW, Sheets HD (2005) Shape based assignments tests suggest transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae). Front Zool 2:11

    Article  PubMed  Google Scholar 

  • Polly PD (2005) Development and phenotypic correlations: the evolution of tooth shape in Sorex araneus. Evolut Develop 7:29–41

    Article  Google Scholar 

  • Rego C, Matos M, Santos M (2006) Symmetry breaking in interspecific Drosophila hybrids is not due to developmental noise. Evolution 60(4):746–761

    PubMed  Google Scholar 

  • Renaud S, Michaux JR (2003) Adaptive latitudinal trends in the mandible shape of Apodemus wood mice. J Biogeogr 30:1617–1628

    Article  Google Scholar 

  • Renaud S, Auffray J-C (2009) Adaptation and plasticity in insular evolution of the house mouse mandible. J Zool Syst Evol Res (in press)

  • Renaud S, Auffray J-C, Michaux J (2006) Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Evolution 60:1701–1717

    PubMed  Google Scholar 

  • Renaud S, Chevret P, Michaux J (2007) Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents. Zool Scr 36:525–535

    Article  Google Scholar 

  • Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372

    Article  PubMed  Google Scholar 

  • Rieseberg LH, Widmer A, Arntz AM, Burke JM (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos Trans R Soc Lond B 358:1141–1147

    Article  CAS  Google Scholar 

  • Sage RD, Atchley WR, Capanna E (1993) House mice as models in systematic biology. Syst Biol 42(4):523–561

    Google Scholar 

  • Satoh K (1997) Comparative functional morphology of mandibular forward movement during mastication of two murid rodents, Apodemus speciosus (Murinae) and Clethrionomys rufocanus (Arvicolinae). J Morphol 231:131–142

    Article  PubMed  CAS  Google Scholar 

  • Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774

    Article  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207

    Article  PubMed  Google Scholar 

  • Thorpe RS, Leamy L (1983) Morphometric studies in inbred and hybrid House mice (Mus sp.): multivariate analysis of size and shape. J Zool Lond 199:421–432

    Article  Google Scholar 

  • Valentin A, Sévigny J-M, Chanut J-P (2002) Geometric morphometrics reveals body shape differences between sympatric redfish Sebastes mentella, Sebastes fasciatus and their hybrids in the Gulf of St Lawrence. J Fish Biol 60:857–875

    Google Scholar 

  • Wilde GR, Echelle AA (1997) Morphological variation in intergrade pupfish populations from the Pecos River, Texas, U.S.A. J Fish Biol 50:523–539

    Article  Google Scholar 

  • Zelditch ML, Wood AR, Bonett RM, Swiderski DL (2008) Modularity of the rodent mandible: integrating bones, muscles, and teeth. Evol Dev 10:756–766

    PubMed  Google Scholar 

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Acknowledgements

We would like to thank F. Fel-Clair, K. Manolakou, A. Orth and A. Zaegek for help and technical assistance during the rearing of the animals. We also thank the GDR 2474 CNRS “Morphométrie et Evolution des Formes” for financial support in the last steps of the work. This is contribution ISEM 2009-059.

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Correspondence to Sabrina Renaud.

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Renaud, S., Alibert, P. & Auffray, JC. Mandible shape in hybrid mice. Naturwissenschaften 96, 1043–1050 (2009). https://doi.org/10.1007/s00114-009-0563-4

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  • DOI: https://doi.org/10.1007/s00114-009-0563-4

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