期刊论文详细信息
BMC Evolutionary Biology
Modularity as a source of new morphological variation in the mandible of hybrid mice
Jean-Christophe Auffray3  Paul Alibert1  Sabrina Renaud2 
[1] Biogéosciences, CNRS, Université de Bourgogne, 21000, Dijon, France;Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, CNRS, Université Lyon 1, 69622, Villeurbanne, France;Institut des Sciences de l’Evolution, CNRS, Université Montpellier 2, 34095, Montpellier, France
关键词: Transgressive phenotypes;    Geometric morphometrics;    Hybridization;    Mandible shape;    House mouse;    Mus musculus;   
Others  :  1140578
DOI  :  10.1186/1471-2148-12-141
 received in 2012-02-10, accepted in 2012-07-17,  发布年份 2012
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【 摘 要 】

Background

Hybridization is often seen as a process dampening phenotypic differences accumulated between diverging evolutionary units. For a complex trait comprising several relatively independent modules, hybridization may however simply generate new phenotypes, by combining into a new mosaic modules inherited from each parental groups and parts intermediate with respect to the parental groups. We tested this hypothesis by studying mandible size and shape in a set of first and second generation hybrids resulting from inbred wild-derived laboratory strains documenting two subspecies of house mice, Musmusculus domesticus and Musmusculus musculus. Phenotypic variation of the mandible was divided into nested partitions of developmental, evolutionary and functional modules.

Results

The size and shape of the modules were differently influenced by hybridization. Some modules seemed to be the result of typical additive effects with hybrids intermediate between parents, some displayed a pattern expected in the case of monogenic dominance, whereas in other modules, hybrids were transgressive. The result is interpreted as the production of novel mandible morphologies. Beyond this modularity, modules in functional interaction tended to display significant covariations.

Conclusions

Modularity emerges as a source of novel morphological variation by its simple potential to combine different parts of the parental phenotypes into a novel offspring mosaic of modules. This effect is partly counterbalanced by bone remodeling insuring an integration of the mosaic mandible into a functional ensemble, adding a non-genetic component to the production of transgressive phenotypes in hybrids.

【 授权许可】

   
2012 Renaud et al.; licensee BioMed Central Ltd.

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