Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals

EvoDevo

Marcelo R Sánchez-Villagra⁵  Motokazu Ando¹  Kazuhiko Koyasu²  Sen-ichi Oda⁶  Christoph PE Zollikofer⁷  Kenneth C Catania³  Gen Suwa⁴  Christian Mitgutsch⁵  Hideki Endo⁴  Daisuke Koyabu⁴ 

[1] Faculty of Agriculture, Tokyo University of Agriculture, Funako 1737, 243-0034 Atsugi, Japan;The Second Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Kusumotochou 1-100, 464-8650 Nagoya, Japan;Department of Biological Sciences, Vanderbilt University, VU Station B, Box 35-1634, Nashville, USA;The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, 113-0033 Tokyo, Japan;Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland;Department of Zoology, Okayama University of Science, Ridaichou, Kita-ku, 700-0005 Okayama, Japan;Anthropologisches Institut, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland

关键词: micro CT;    phylogeny;    integration;    ossification;    embryology;    Eulipotyphla;    heterochrony;    skull;   

Others  :  810658
DOI  :  10.1186/2041-9139-2-21

 received in 2011-07-05, accepted in 2011-11-01,  发布年份 2011

【 摘 要 】

Background

Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development.

Results

An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification).

Conclusions

The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.

【 授权许可】

   
2011 Koyabu et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Richardson MK, Jeffery JE, Coates MI, Bininda-Emonds ORP: Comparative methods in developmental biology. Zoology 2001, 104:278-283.
• [2]Maxwell EE, Harrison LB: Methods for the analysis of developmental sequence data. Evol Dev 2009, 11:109-119.
• [3]de Jong IML, Colbert MW, Witte F, Richardson MK: Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid. Evol Dev 2009, 11:625-635.
• [4]de Jong IML, Witte F, Richardson MK: Developmental stages until hatching of the Lake Victoria cichlid Haplochromis piceatus (Teleostei: Cichlidae). J Morphol 2009, 270:519-535.
• [5]Mitgutsch C, Wimmer C, Sánchez-Villagra MR, Hahnloser R, Schneider RA: Timing of ossification in duck, quail, and zebra finch: intraspecific variation, heterochronies, and life histgory evolution. Zoolog Sci 2011, 28:491-500.
• [6]Sánchez-Villagra MR, Goswami A, Weisbecker V, Mock O, Kuratani S: Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evol Dev 2008, 10:519-530.
• [7]Springer MS, de Jong WW: Which mammalian supertree to bark up? Science 2001, 291:1709.
• [8]Wilson LAB, Schradin C, Mitgutsch C, Galliari FC, Mess A, Sánchez-Villagra MR: Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia). Org Divers Evol 2010, 10:243-258.
• [9]Goswami A: Cranial modularity and sequence heterochrony in mammals. Evol Dev 2007, 9:290-298.
• [10]Goswami A, Weisbecker V, Sánchez-Villagra MR: Developmental modularity and the marsupial-placental dichotomy. J Exp Zool B Mol Dev Evol 2009, 312:186-195.
• [11]Schoch RR: Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades. Evol Dev 2006, 8:524-536.
• [12]Shubin NH, Davis MC: Modularity in the evolution of vertebrate appendages. In Modularity in Development and Evolution. Edited by Schlosser G, Wagner GP. Chicago, IL: University of Chicago Press; 2004:429-440.
• [13]Harrison LB, Larsson HCE: Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony. Syst Biol 2008, 57:378-387.
• [14]Blomquist GE: Methods of sequence heterochrony for describing modular developmental changes in human evolution. Am J Phys Anthropol 2008, 138:231-238.
• [15]Olson ME, Rosell JA: Using heterochrony to detect modularity in the evolution of stem diversity in the plant family Moringaceae. Evolution 2006, 60:724-734.
• [16]Schmidt K, Starck JM: Developmental variability during early embryonic development of zebra fish, Danio rerio. J Exp Zool B Mol Dev Evol 2004, 302:446-457.
• [17]Hendrikse JL, Parsons TE, Hallgrímsson B: Evolvability as the proper focus of evolutionary developmental biology. Evol Dev 2007, 9:393-401.
• [18]Müller GB: Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 2007, 8:943-949.
• [19]Wagner GP, Pavlicev M, Cheverud JM: The road to modularity. Nat Rev Genet 2007, 8:921-931.
• [20]Hallgrímsson B, Lieberman DE: Mouse models and the evolutionary developmental biology of the skull. Integr Comp Biol 2008, 48:373.
• [21]Pigliucci M: Is evolvability evolvable? Nat Rev Genet 2008, 9:75-82.
• [22]Klingenberg CP: Developmental constraints, modules and evolvability. In Variation: A Central Concept in Biology. Edited by Hallgrímsson B, Hall BK. Amsterdam, Netherlands: Elsevier; 2005:219-247.
• [23]Wagner GP: Homologues, natural kinds and the evolution of modularity. Am Zool 1996, 36:36-43.
• [24]Badyaev AV, Foresman KR, Young RL: Evolution of morphological integration: developmental accommodation of stress-induced variation. Am Nat 2005, 166:382-395.
• [25]Cheverud JM: Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 1982, 36:499-516.
• [26]Cheverud JM: Developmental integration and the evolution of pleiotropy. Am Zool 1996, 36:44-50.
• [27]Cheverud JM, Ehrich TH, Vaughn TT, Koreishi SF, Linsey RB, Pletscher LS: Pleiotropic effects on mandibular morphology II: differential epistasis and genetic variation in morphological integration. J Exp Zool B Mol Dev Evol 2004, 302:424-435.
• [28]Cheverud JM, Rutledge JJ, Atchley WR: Quantitative genetics of development: genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution 1983, 37:895-905.
• [29]Zelditch ML: Ontogenetic variation in patterns of developmental and functional integration in the laboratory rat. Evolution 1988, 42:28-41.
• [30]Zelditch ML, Moscarella RA: Form, function and life history: spatial and temporal dynamics of integration. In Phenotypic Integration. Edited by Pigliucci M, Preston K. Oxford, United Kingdom: Oxford University Press; 2004:274-301.
• [31]Klingenberg CP, Leamy LJ, Cheverud JM: Integration and modularity of quantitative trait locus effects on geometric shape in the mandible. Genetics 2003, 166:1909-1921.
• [32]Klingenberg CP, Mebus K, Auffray JC: Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evol Dev 2003, 5:522-531.
• [33]Marroig G, Shirai LT, Porto A, de Oliveira FB, De Conto V: The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol Biol 2009, 36:136-148.
• [34]Porto A, de Oliveira FB, Shirai LT, De Conto V, Marroig G: The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol Biol 2009, 36:118-135.
• [35]Kaji T, Tsukagoshi A: Heterochrony and modularity in the degeneration of maxillopodan nauplius eyes. Biol J Linn Soc 2010, 99:521-529.
• [36]de Beer GR: The Development of the Vertebrate Skull. London: Oxford University Press; 1937.
• [37]Gould SJ: Ontogeny and Phylogeny. Cambridge, MA: Harvard University Press; 1977.
• [38]Raff EC, Raff RA: Dissociability, modularity, evolvability. Evol Dev 2000, 2:235-237.
• [39]Poe S: A test for patterns of modularity in sequences of developmental events. Evolution 2004, 58:1852-1855.
• [40]Klingenberg CP: Integration, modules and development: molecules to morphology to evolution. In Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes. Edited by Pigliucci M, Preston K. Oxford, United Kingdom: Oxford University Press; 2004:213-230.
• [41]Asher RJ, Helgen KM: Nomenclature and placental mammal phylogeny. BMC Evol Biol 2010, 10:102. BioMed Central Full Text
• [42]Goswami A, Prochel J: Ontogenetic morphology and allometry of the cranium in the common european mole (Talpa europaea). J Mammal 2007, 88:667-677.
• [43]Prochel J, Goswami A, David Carmona F, Jimenéz R: Ossification sequence in the mole Talpa occidentalis (Eulipotyphla, Talpidae) and comparison with other mammals. Mammal Biol 2008, 73:399-403.
• [44]Frick H: Die Entwicklung und Morphologie des Chondrokraniums von Myotis Kaup. Stuttgart, Germany: Georg Thieme Verlag; 1954.
• [45]Strong RM: The order, time, and rate of ossification of the albino rat (Mus norvegicus albinus) skeleton. Am J Anat 1925, 36:313-355.
• [46]Zeller U: Morphogenesis of the mammalian skull with special reference to Tupaia. In Mammalia Depicta. Edited by Kuhn HX, Zeller U. Hamburg/Berlin, Germany: Verlag Paul Parey; 1987:17-50.
• [47]Sánchez-Villagra MR, Horovitz I, Motokawa M: A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships. Cladistics 2006, 22:59-88.
• [48]Amrine-Madsen H, Koepfli KP, Wayne RK, Springer MS: A new phylogenetic marker, apolipoprotein B, provides compelling evidence for eutherian relationships. Mol Phylogenet Evol 2003, 28:225-240.
• [49]Dubey S, Salamin N, Ohdachi SD, Barrière P, Vogel P: Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations. Mol Phylogenet Evol 2007, 44:126-137.
• [50]Ohdachi SD, Hasegawa M, Iwasa MA, Vogel P, Oshida T, Lin LK, Abe H: Molecular phylogenetics of soricid shrews (Mammalia) based on mitochondrial cytochrome b gene sequences: with special reference to the Soricinae. J Zool 2006, 270:177-191.
• [51]Shinohara A, Campbell KL, Suzuki H: Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds. Mol Phylogenet Evol 2003, 27:247-258.
• [52]Shinohara A: Molecular phylogeny and phylogeography of the family Talpidae (Eulipotyphla Mammalia). PhD thesis. Hokkaido University Graduate School of Environmental Earth Science; 2008.
• [53]Weisbecker V, Goswami A, Wroe S, Sánchez-Villagra MR: Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 2008, 62:2027-2041.
• [54]Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ: Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Natl Acad Sci USA 2010, 107:18903-18908.
• [55]Jeffery JE, Bininda-Emonds ORP, Coates MI, Richardson MK: A new technique for identifying sequence heterochrony. Syst Biol 2005, 54:230.
• [56]Nunn CL, Smith KK: Statistical analyses of developmental sequences: the craniofacial region in marsupial and placental mammals. Am Nat 1998, 152:82-101.
• [57]Schulmeister S, Wheeler WC: Comparative and phylogenetic analysis of developmental sequences. Evol Dev 2004, 6:50-57.
• [58]Jeffery JE, Bininda-Emonds ORP, Coates MI, Richardson MK: Analyzing evolutionary patterns in amniote embryonic development. Evol Dev 2002, 4:292-302.
• [59]Hautier L, Weisbecker V, Goswami A, Knight F, Kardjilov N, Asher RJ: Skeletal ossification and sequence heterochrony in xenarthran evolution. Evol Dev, in press.
• [60]Bininda-Emonds ORP, Jeffrey JE, Richardson MK: Is sequence heterochrony an important evolutionary mechanism in mammals? J Mamm Evol 2003, 10:335-361.
• [61]Swofford DL: PAUP: Phylogenetic Analysis Using Parsimony, version 4.0 b10. Sunderland. 2001.
• [62]Noden DM, Trainor PA: Relations and interactions between cranial mesoderm and neural crest populations. J Anat 2005, 207:575-601.
• [63]Hall BK: Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. New York: Academic Press; 2005.
• [64]Cheverud JM: Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. Am Nat 1995, 145:63-89.
• [65]Marroig G, Cheverud JM: A comparison of phenotypic variation and covariation patterns and the role of phylogeny ecology and ontogeny during cranial evolution of New World monkeys. Evolution 2001, 55:2576-2600.
• [66]Felsenstein J: Phylogenies and the comparative method. Am Nat 1985, 125:1-15.
• [67]Hood G: PopTools. Canberra: Pest Animal Control CRC; 2000.
• [68]Hammer Ø, Harper DAT, Ryan PD: PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 2001, 4:9.
• [69]Weisbecker V, Mitgutsch C: A large-scale survey of heterochrony in anuran cranial ossification patterns. J Zool Syst Evol Res 2010, 48:332-347.
• [70]Smith KK: Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 1997, 51:1663-1678.
• [71]Novacek MJ: Patterns of diversity in the mammalian skull. In The Skull: Patterns of Structural and Systematic Diversity. Volume 2. Edited by Hanken J, Hall BK. Chicago, IL: University of Chicago Press; 1993::438-545.
• [72]Hornaday WT: The American Natural History: A Foundation of Useful Knowledge of the Higher Animals of North America. New York, NY: Charles Scribner's Sons; 1904.
• [73]Yalden DW: The anatomy of mole locomotion. J Zool 1966, 149:55-64.
• [74]Catania KC: Epidermal sensory organs of moles, shrew moles, and desmans: a study of the family talpidae with comments on the function and evolution of Eimer's organ. Brain Behav Evol 2000, 56:146-174.
• [75]Shibanai S: Ultrastructure of the Eimer's organs of the Japanese shrew mole, Urotrichus talpoides (Insectivora, Mammalia) and their changes following infraorbital axotomy. Anat Anz 1988, 165:105-129.
• [76]Catania KC: A comparison of the Eimer's organs of three north american moles: the hairy-tailed mole (Parascalops breweri), the star-nosed mole (Condylura cristata), and the eastern mole (Scalopus aquaticus). J Comp Neurol 1995, 354:150-160.
• [77]Catania KC, Kaas JH: Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation. J Comp Neurol 1997, 387:215-233.
• [78]Abe H: Insectivores and xenathrans. In The Planet of Animals. Volume 39. Edited by Abe H, Imafuku M. Tokyo, Japan: Asahi Shinbun; 1992::66-96.
• [79]Abe H: Illustrated Skulls of Japanese Mammals. Sapporo: Hokkaido University Press; 2000.
• [80]Ishii N: Urotrichus talpoides Temminck, 1841. In The Wild Mammals of Japan. Edited by Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T. Kyoto, Japan: Shoukadoh Kyoto; 2009.
• [81]Whidden HP: Comparative myology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla). Am Mus Nov 2000, 3294:1-53.
• [82]Mitgutsch C, Richardson MK, Jiménez R, Martin JE, Kondrashov P, de Bakker MAG, Sánchez-Villagra MR: Circumventing the polydactyly 'constraint': the mole's 'thumb'. Biol Lett, in press.
• [83]Edwards LF: Morphology of the forelimb of the mole (Scalops aquaticus, L.) in relation to its fossorial habits. Ohio J Sci 1937, 37:20-41.
• [84]Starck D: Lehrbuch der speziellen Zoologie. Wirbeltiere. Teil 5: Säugetiere. Jena, Germany: Gustav Fischer; 1995.
• [85]Catania KC: Olfaction: underwater 'sniffing' by semi-aquatic mammals. Nature 2006, 444:1024-1025.
• [86]McIntyre IW, Campbell KL, MacArthur RA: Body oxygen stores, aerobic dive limits and diving behaviour of the star-nosed mole (Condylura cristata) and comparisons with non-aquatic talpids. J Exp Biol 2002, 205:45-54.
• [87]Abe H: Chimarrogale platycephala (Temminck, 1842). In The Wild Mammals of Japan. Edited by Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T. Kyoto, Japan: Shoukadoh; 2009:16-17.
• [88]Douady CJ, Douzery EJP: Molecular estimation of eulipotyphlan divergence times and the evolution of. Mol Phylogenet Evol 2003, 28:285-296.
• [89]Douady CJ, Douzery EJP: Hedgehogs, shrews, moles, and solenodons (Eulipotyphla). In The Timetree of Life. Volume 157. Edited by Hedges SB, Kumar S. New York, NY: Oxford University Press; 2009::1011-1018.
• [90]MacPhee RDE, Novacek MJ: Definition and relationships of Lipotyphla. In Mammal Phylogeny: Placentals. Edited by Szalay FS, Novacek MJ, McKenna MC. New York: Springer-Verlag; 1993:13-31.
• [91]Sánchez-Villagra MR: Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. J Exp Zool B Mol Dev Evol 2002, 294:264-273.
• [92]Davies M: Ontogeny of bone and the role of heterochrony in the myobatrachine genera Uperoleia, Crinia, and Pseudophryne (Anura: Leptodactylidae: Myobatrachinae). J Morphol 1989, 200:269-300.
• [93]Mabee PM, Olmstead KL, Cubbage CC: An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 2000, 54:2091-2106.
• [94]Rieppel O: Studies on skeleton formation in reptiles, v. Patterns of ossification in the skeleton of Alligator mississippiensis Daudin (Reptilia, Crocodylia). Zool J Linn Soc 1993, 109:301-325.
• [95]Goswami A: Cranial modularity shifts during mammalian evolution. Am Nat 2006, 168:270-280.
• [96]Smith KK: Integration of craniofacial structures during development in mammals. Am Zool 1996, 36:70-79.