Revisiting de Beer’s textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronic growth, and underlies morphological innovation in the jaws of belonoid fishes

EvoDevo

Axel Meyer²  Claudia Koppermann²  Helen M Gunter¹ 

[1] Zukunftskolleg, University of Konstanz, Universitätstrasse 10, 78457 Constance, Germany;Department of Biology, Lehrstuhl für Zoologie und Evolutionsbiologie, University of Konstanz, Universitätstrasse 10, 78457 Constance, Germany

关键词: Calmodulin;    Medaka;    Belone;    Dermogenys;    Gavin de Beer;    Beloniformes;    Jaw development;    Morphological innovation;    Heterochrony;   

Others  :  802116
DOI  :  10.1186/2041-9139-5-8

 received in 2013-08-12, accepted in 2013-12-12,  发布年份 2014

【 摘 要 】

Background

Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. Understanding the nature of these developmental events can provide insights into fundamental molecular mechanisms of evolutionary change. Fishes from the Suborder Belonoidei display a vast array of extreme craniofacial morphologies that appear to have arisen through a series of heterochronic shifts. We performed a molecular heterochrony study, comparing postembryonic jaw development in representatives of the Suborder Belonoidei, the halfbeak Dermogenys pusilla (where the lower jaw is considerably elongated compared to the upper jaw) and the needlefish Belone belone (where both jaws are elongated), to a representative of their sister group the Suborder Adrianichthyoidei, the medaka Oryzias latipes, which has retained the ancestral morphology.

Results

Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony. We identified toothless extensions of the dentaries as innovations of Belonoid fishes and the source of heterochronic growth. The molecular basis of growth heterochronies in the Belonoidei was examined through comparing expression of skeletogenic genes during development of halfbeak and medaka. The calmodulin paralogue calm1 was identified as a potential regulator of jaw length in halfbeak as its expression gradually increases in the lower jaw, but not the upper jaw, in a pattern that matches its outgrowth. Moreover, medaka displays equal expression of calm1 in the upper and lower jaws, consistent with the lack of jaw outgrowth in this species.

Conclusions

Heterochronic shifts in jaw growth have occurred repeatedly during the evolution of Belonoid fishes and we identify toothless extensions of the dentaries as an important innovation of this group. Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.

【 授权许可】

   
2014 Gunter 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]Carroll SB: Endless Forms Most Beautiful: The New Science of Evo Devo. London: W. W. Norton & Company; 2005.
• [2]de Beer GR: Embryos and Ancestors. London: Oxford University Press; 1940.
• [3]Gould SJ: Ontogeny and Phylogeny. Cambridge: Mass: Belknap Press of Harvard University Press; 1977.
• [4]Raff RA, Wray GA: Heterochrony: developmental mechanisms and evolutionary results. J Evol Biol 1989, 2:409-434.
• [5]Rice SH: The analysis of ontogenetic trajectories: when a change in size or shape is not heterochrony. Proc Natl Acad Sci U S A 1997, 94:907-912.
• [6]Klingenberg CP: Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 1998, 73:79-123.
• [7]Smith KM: Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc 2001, 73:169-186.
• [8]Smith KK: Time’s arrow: heterochrony and the evolution of development. Int J Dev Biol 2003, 47:613-621.
• [9]Alberch P, Gould SJ, Oster GF, Wake DB: Size and shape in ontogeny and phylogeny. Paleobiology 1979, 5:296-317.
• [10]Raff EC, Raff RA: Dissociability, modularity, evolvability. Evol Dev 2000, 2:235-237.
• [11]Hall BK: Developmental processes underlying heterochrony as an evolutionary mechanism. Can J Zool 1984, 62:1-7.
• [12]Yamamoto Y, Jeffery WR: Central role for the lens in cave fish eye degeneration. Science 2000, 289:631-633.
• [13]Carleton KL, Spady TC, Streelman JT, Kidd MR, McFarland WN, Loew ER: Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol 2008, 6:22. BioMed Central Full Text
• [14]Albertson RC, Yan YL, Titus TA, Pisano E, Vacchi M, Yelick PC, Detrich HW, Postlethwait JH: Molecular pedomorphism underlies craniofacial skeletal evolution in Antarctic notothenioid fishes. BMC Evol Biol 2010, 10:4. BioMed Central Full Text
• [15]Kerney R, Gross JB, Hanken J: Early cranial patterning in the direct-developing frog Eleutherodactylus coqui revealed through gene expression. Evol Dev 2010, 12:373-382.
• [16]Hall BK: Evo-Devo: evolutionary developmental mechanisms. Int J Dev Biol 2003, 47(7/8):491-496.
• [17]Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ: The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 2006, 442:563-567.
• [18]Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ: Bmp4 and morphological variation of beaks in Darwin’s finches. Science 2004, 305:1462-1465.
• [19]Grant PR, Grant BR, Abzhanov A: A developing paradigm for the development of bird beaks. Biol J Linn Soc 2006, 88:17-22.
• [20]Albertson RC, Kocher TD: Genetic and developmental basis of cichlid trophic diversity. Heredity 2006, 97:211-221.
• [21]Albertson RC, Streelman JT, Kocher TD, Yelick PC: Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proc Natl Acad Sci U S A 2005, 102:16287-16292.
• [22]Parsons KJ, Albertson RC: Roles for Bmp4 and CaM1 in shaping the jaw: evo-devo and beyond. Annu Rev Genet 2009, 43:369-388.
• [23]Boughton DA, Collette BB, McCune AR: Heterochrony in jaw morphology of the needlefishes (Teleostei: Belonidae). Syst Zool 1991, 40:329-354.
• [24]Schlesinger Z: Zur phylogenie und ethologie der Scombresociden. Verh Zool-Bot Ges Wien 1909, 59:302-339.
• [25]Regan CT: The classification of the teleostean fishes of the order Synentognathi. Ann Mag N Hist 1911, 7:327-335.
• [26]Nichols JT, Breder CMJ: An annotated list of the Synentognathi with remarks on their development and relationships. Zoologica (N Y) 1928, 8:423-448.
• [27]Lovejoy NR, Iranpour M, Collette BB: Phylogeny and jaw ontogeny of beloniform fishes. Integr Comp Biol 2004, 44:366-377.
• [28]Levit GS, Hossfeld U, Olsson L: The integration of Darwinism and evolutionary morphology: Alexej Nikolajevich Severtzoff (1866 to 1936) and the developmental basis of evolutionary change. J Exp Zool Part B 2004, 302B:343-354.
• [29]Severtzoff AN: Über die beziehung zwischen der ontogenese und der phylogenese der tiere. Jena Zeitrschr Naturwiss 1927, 63:51-180.
• [30]Lovejoy NR: Reinterpreting recapitulation: systematics of needlefishes and their allies (Teleostei: Beloniformes). Evolution 2000, 54(4):1349-1362.
• [31]Parenti L: A phylogenetic analysis and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae). Zool J Linn Soc-Lond 2008, 154:494-610.
• [32]Hansen TF: The evolution of genetic architecture. Ann Rev Ecol Evol Syst 2006, 37:123-157.
• [33]Near TJ, Dornburg A, Eytan RI, Keck BP, Smith WL, Khun KL, Moore JA, Price SA, Burbrink FT, Friedman M, et al.: Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proc Natl Acad Sci U S A 2013, 110:12738-12743.
• [34]Kinoshita M, Murata K, Naruse K, Tanaka M: A Laboratory Manual for Medaka Biology. 1st edition. Wiley-Blackwell: Ames, Iowa, USA; 2009.
• [35]Walker MB, Kimmel CB: A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 2007, 82:23-28.
• [36]Gould SJ: Of coiled oysters and big brains: how to rescue the terminology of heterochrony, now gone astray. Evol Dev 2000, 2(5):241-248.
• [37]Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ: Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191.
• [38]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
• [39]Hurst LD: The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 2002, 18(9):486-487.
• [40]Yang Z, PAML4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol 24:1586-1591.
• [41]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17(1):32-43.
• [42]Amplifx 1.5.4http://ifrjr.nord.univ-mrs.fr/AmplifX-Home-page webcite
• [43]Cummings ME, Larkins-Ford J, Reilly CR, Wong RY, Ramsey M, Hofmann HA: Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc Biol Sci 2008, 275:393-402.
• [44]Simon P: Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 2003, 19:1439-1440.
• [45]Gunter HM, Fan S, Xiong F, Franchini P, Fruciano C, Meyer A: Shaping development through mechanical strain: the transcriptional basis of diet-dependent phenotypic plasticity in a cichlid fish. Mol Ecol 2013, 22:4516-4531.
• [46]Mitteroecker P, Gunz P, Weber G, Bookstein F: Regional dissociated heterochrony in multivariate analysis. Ann Anat 2004, 186(5):463-470.
• [47]Clemen G, Wanninger AC, Greven H: The development of the dentigerous bones and teeth in the hemiramphid fish Dermogenys pusillus (Atheriniformes, Teleostei). Ann Anat 1997, 179:165-174.
• [48]Kuzir S, Kozaric Z, Gjurcevic E, Bazdaric B, Petrinec Z: Osteological development of the garfish (Belone belone) larvae. Anat Histol Embryol 2009, 38:351-354.
• [49]Langille RM, Hall BK: Development of the head skeleton of the Japanese medaka, Oryzias latipes (Teleostei). J Morphol 1987, 193:135-158.
• [50]Greven H, Wanninger AC, Clemen G: Dentigerous bones and dentition in the hemiramphid fish Dermogenys pusillus (Atheriniformes, Teleostei). Ann Anat 1997, 179:21-32.
• [51]Lovejoy N: Phylogeny and ontogeny of needlefishes. Integr Comp Biol 2000, 42:1268-1268.
• [52]Kirschner M, Gerhart J: Evolvability. Proc Natl Acad Sci U S A 1998, 95:8420-8427.
• [53]Collette BB, McGowen GE, Parin NV, Mito S: Beloniformes: development and relationships. Am Soc Ichthyologists and Herpetologists 1984, 1:335-354.
• [54]Meisner AD: Phylogenetic systematics of the viviparous halfbeak genera Dermogenys and Nomorhamphus (Teleostei: Hemiramphidae: Zenarchopterinae). Zool J Linn Soc 2001, 133:199-283.
• [55]Wise SB, Stock DW: Conservation and divergence of Bmp2a, Bmp2b, and Bmp4 expression patterns within and between dentitions of teleost fishes. Evol Dev 2006, 8:511-523.
• [56]Zayzafoon M: Calcium/calmodulin signaling controls osteoblast growth and differentiation. J Cell Biochem 2006, 97(1):56-70.
• [57]Choi YH, Choi J-H, Oh J-W, Lee K-Y: Calmodulin-dependent kinase II regulates osteoblast differentiation through regulation of osterix. Biochem Bioph Res Co 2013, 432:248-255.
• [58]Seo JH, Jin Y-H, Jeong HM, Kim Y-J, Jeong HG, Yeo C-Y, Lee K-Y: Calmodulin-dependent kinase II regulates Dlx5 during osteoblast differentiation. Biochem Bioph Res Co 2009, 384(1):100-104.
• [59]Toutenhoofd SL, Strehler EE: The calmodulin multigene family as a unique case of genetic redundancy: multiple levels of regulation to provide spatial and temporal control of calmodulin pools? Cell Calcium 2000, 28:83-96.
• [60]Nojima H: Structural organization of multiple rat calmodulin genes. J Mol Biol 1989, 208:269-282.
• [61]Matsuo K, Sato K, Ikeshima H, Shimoda K, Takano T: Four synonymous genes encode calmodulin in the teleost fish, medaka (Oryzias latipes): conservation of the multigene one-protein principle. Gene 1992, 119:279-281.
• [62]Berchtold MW, Egli R, Rhyner JA, Hameister H, Strehler EE: Localization of the human bona fide calmodulin genes CALM1, CALM2, and CALM3 to chromosome-14q24–Q31, chromosome-2p21.1–P21.3, and chromosome-19q13.2–Q13.3. Genomics 1993, 16:461-465.
• [63]Friedberg F, Taliaferro LT: Calmodulin genes in zebrafish (revisited). Mol Biol Rep 2005, 32:55-60.
• [64]Luan J, Liu ZH, Zhang SC, Li HY, Fan CX, Li L: Characterization, evolution and expression of the calmodulin1 genes from the amphioxus Branchiostoma belcheri tsingtauense. Acta Bioch Bioph Sin 2007, 39:255-264.
• [65]Berry F, Brown IR: Developmental expression of calmodulin mRNA and protein in regions of the postnatal rat brain. J Neurosci Res 1995, 42:613-622.
• [66]Ni B, Landry CF, Brown IR: Developmental expression of neuronal calmodulin mRNA species in the rat brain analyzed by in situ hybridization. J Neurosci Res 1992, 33:559-567.
• [67]Weinman J, Della Gaspera B, Dautigny A, Pham Dinh D, Wang J, Nojima H, Weinman S: Developmental regulation of calmodulin gene expression in rat brain and skeletal muscle. Cell Regul 1991, 2:819-826.
• [68]Landry CF, Ivy GO, Brown IR: Effect of a discrete dorsal forebrain lesion in the rat on the expression of neuronal and glial-specific genes: induction of calmodulin, NF-L, SC1, and GFAP mRNA. J Neurosci Res 1992, 32:280-289.
• [69]Ni B, Brown IR: Modulation of a neuronal calmodulin mRNA species in the rat brain stem by reserpine. Neurochem Res 1993, 18:185-192.
• [70]Whitfield JF, Boynton AL, Macmanus JP, Rixon RH, Sikorska M, Tsang B, Walker PR: The roles of calcium and cyclic AMP in cell proliferation. Ann NY Acad Sci 1980, 339:216-240.
• [71]Godwin SL, Soltoff SP: Extracellular calcium and platelet-derived growth factor promote receptor-mediated chemotaxis in osteoblasts through different signaling pathways. J Biol Chem 1997, 272:11307-11312.
• [72]Yamaguchi T, Chattopadhyay N, Kifor O, Butters RR, Sugimoto T, Brown EM: Mouse osteoblastic cell line (MC3T3-E1) expresses extracellular calcium (Ca-0(2+))-sensing receptor and its agonists stimulate chemotaxis and proliferation of MC3T3-E1 cells. J Bone Miner Res 1998, 13:1530-1538.