Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes

EvoDevo

Jacqueline F Webb¹  Nathan C Bird¹ 

[1] Current address: Department of Biological Sciences, University of Rhode Island, 120 Flagg Road, Kingston RI 02881, USA

关键词: Lateral line;    Modularity;    Heterochrony;    Dermatocranium;    Neuromast;    Cichlidae;    Tramitichromis;    Aulonocara;   

Others  :  801068
DOI  :  10.1186/2041-9139-5-21

 received in 2014-02-12, accepted in 2014-05-14,  发布年份 2014

【 摘 要 】

Background

The canals of the mechanosensory lateral line system are components of the dermatocranium, and demonstrate phenotypic variation in bony fishes. Widened lateral line canals evolved convergently in a limited number of families of teleost fishes and it had been hypothesized that they evolved from narrow canals via heterochrony and explore modularity in the lateral line system. Two species of cichlids with different canal phenotypes were used to test a hypothesis of heterochrony. Histological material prepared from ontogenetic series of Aulonocara stuartgranti (widened canals) and Tramitichromis sp. (narrow canals) was analyzed using ANCOVA to determine rates of increase in canal diameter and neuromast size (length, width) and to compare the timing of onset of critical stages in canal morphogenesis (enclosure, ossification).

Results

A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis. However, rates of increase in canal diameter and neuromast size among canals, among canal portions and among canals segments reveal similar trends within both species.

Conclusion

The evolution of widened lateral line canals is the result of dissociated heterochrony - acceleration in the rate of increase of both canal diameter and neuromast size, and delay in the onset of canal morphogenesis, in Aulonocara (widened canals) relative to Tramitichromis (narrow canals). Common rates of increase in canal diameter and neuromast size among canal portions in different dermatocranial bones and among canal segments reflect the absence of local heterochronies, and suggest modular integration among canals in each species. Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found. Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences. Heterochrony can likely explain the convergent evolution of widened lateral line canals among diverse taxa. The lateral line system provides a valuable context for novel analyses of the relationship between developmental processes and the evolution of behaviorally and ecologically relevant phenotypes in fishes.

【 授权许可】

   
2014 Bird and Webb; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Gould SJ: Ontogeny and Phylogeny. Cambridge MA: Harvard University Press; 1977.
• [2]Alberch P, Gould SJ, Oster GF, Wake DB: Size and shape in ontogeny and phylogeny. Paleobiology 1979, 5:296-317.
• [3]Raff RA, Wray GA: Heterochrony: developmental mechanisms and evolutionary results. J Evol Biol 1989, 2:409-434.
• [4]McKinney ML: McNamara KJ: Heterochrony: the evolution of ontogeny . New York: Plenum Press; 1991.
• [5]Klingenberg CP: Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 1998, 73:79-123.
• [6]Raff RA: The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press; 1996.
• [7]Schlosser G, Wagner GP: Modularity in Development and Evolution. Chicago: University of Chicago Press; 2004.
• [8]Mitteroecker P, Gunz P, Weber GW, Bookstein FL: Regional dissociated heterochrony in multivariate analysis. Ann Anat 2004, 186:463-470.
• [9]Smith KK: Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc 2001, 73:169-186.
• [10]Smith KK: Sequence heterochrony and the evolution of development. J Morphol 2002, 252:82-97.
• [11]Smith KK: Time’s arrow: heterochrony and the evolution of development. Int J Dev Biol 2003, 47:613-621.
• [12]McNamara KJ: Shapes of Time: the Evolution of Growth and Development. Baltimore: The Johns Hopkins University Press; 1997.
• [13]Gerber S, Hopkins MJ: Mosaic heterochrony and evolutionary modularity: the trilobite genus Zacanthopsis as a case study. Evolution 2011, 65:3241-3252.
• [14]Bemis WE: Paedomorphosis and the evolution of the Dipnoi. Paleobiology 1984, 10:293-307.
• [15]Boughton DA, Collette BB, McCune AR: Heterochrony in jaw morphology of needlefishes (Teleostei: Belonidae). Syst Zool 1991, 40:329-354.
• [16]Mabee PM, Olmstead KL, Cubbage CC: An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 2000, 54:2091-2106.
• [17]Alberch P, Alberch J: Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander, Bolitoglossa occidentalis (Amphibia: Plethodontidae). J Morphol 1981, 167:249-264.
• [18]Hanken J: Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). I. Osteological variation. Biol J Linn Soc 1984, 23:55-75.
• [19]Schoch R: Heterochrony in the development of the amphibian head. In Evolutionary Change and Heterochrony. Edited by McNamara KJ. Chichester, UK: John Wiley & Sons Ltd; 1995:107-124.
• [20]Bhullar B-AS: A phylogenetic approach to ontogeny and heterochrony in the fossil record: cranial evolution and development in anguimorphan lizards. J Exp Zool (Mol Dev Evol) 2012, 318B:521-530.
• [21]Bhullar B-AS, Marugan-Lobon J, Racimo F, Bever GS, Rowe TB, Norell MA, Abzhanov A: Birds have paedomorphic dinosaur skulls. Nature 2012, 487:223-226.
• [22]Smith KK: Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 1997, 51:1663-1678.
• [23]Sanchez-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.
• [24]Goswami A: Cranial modularity and sequence heterochrony in mammals. Evol Dev 2007, 9:290-298.
• [25]Drake AG: Dispelling dog dogma: an investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape. Evol Dev 2011, 13:204-213.
• [26]Koyabu D, Endo H, Mitgutsch C, Suwa G, Catania KC, Zollikofer CPE, Oda S-I, Koyasu K, Ando M, Sanchez-Villagra MR: Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammal. EvoDevo 2011, 2:21. [http://www.evodevojournal.com/content/2/1/21 webcite] BioMed Central Full Text
• [27]Webb JF: Morphological diversity, development, and evolution of the mechanosensory lateral line system. In The Lateral Line System. Edited by Bleckmann H, Coombs S, Mogdans J. New York: Springer; 2014:17-72.
• [28]Webb JF: Mechanosensory lateral line: Functional morphology and neuroanatomy. In Handbook of Experimental Animals: The Laboratory Fish. Edited by Ostrander G. London: Academic; 2000:236-244.
• [29]Tarby ML, Webb JF: Development of the supraorbital and mandibular lateral line canals in the cichlid, Archocentrus nigrofasciatus. J Morphol 2003, 255:44-57.
• [30]Webb JF, Northcutt RG: Morphology and distribution of pit organs and canal neuromasts in non-teleost bony fishes. Brain Behav Evol 1997, 50:139-151.
• [31]Webb JF, Shirey JE: Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish. Dev Dyn 2003, 228:370-385.
• [32]Webb JF: Lateral line morphology and development and implications for the functional ontogeny of flow sensing of fishes. In Flow Sensing in Air and Water - Behavioural, Neural and Engineering Principles of Operation. Edited by Bleckmann H, Mogdans J, Coombs S. New York: Springer; 2014:247-270.
• [33]Webb JF: Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes. Brain Behav Evol 1989, 33:34-53.
• [34]Denton EJ, Gray JAB: Mechanical factors in the excitation of the lateral lines of fishes. In Sensory Biology of Aquatic Animals. Edited by Atema J, Fay RR, Popper AN, Tavolga WN. New York: Springer; 1988:595-618.
• [35]Denton EJ, Gray JAB: Some observations on the forces acting on neuromasts in fish lateral line canals. In The Mechanosensory Lateral Line: Neurobiology and Evolution. Edited by Coombs S, Görner P, Münz H. New York: Springer; 1989:79-97.
• [36]Schwalbe MAB, Bassett DK, Webb JF: Feeding in the dark: lateral-line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti. J Exp Biol 2012, 21:2060-2071.
• [37]Schwalbe MAB, Webb JF: Sensory basis for detection of benthic prey in two Lake Malawi cichlids. Zoology (Jena) 2014, 117:112-121.
• [38]Webb JF: Developmental constraints and evolution of the lateral line system in teleost fishes. In The Mechanosensory Lateral Line – Neurobiology and Evolution. Edited by Coombs S, Gorner P, Munz H. New York: Springer; 1989:79-98.
• [39]Fryer G, Iles TD: The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver and Boyd: Edinburgh; 1972.
• [40]Greenwood PH: The Haplochromine Fishes of the East African Lakes. Ithaca NY: Cornell University Press; 1981.
• [41]Trewavas E: Tilapiine Fishes of the Genera Sarotherodon, Oreochromis, and Danakilia. London: British Museum (Natural History); 1983.
• [42]Branson BA: The lateral-line system in the Rio Grande perch, Cichlasoma cyanoguttatum (Baird and Girard). Am Midl Nat 1961, 65:446-458.
• [43]Peters HM: Anatomie und entwicklungsgeschichte des lateralissystems von Tilapia (Pisces, Cichlidae). Z Morphol Tiere 1973, 74:89-161.
• [44]Webb JF: Neuromast morphology and lateral line trunk ontogeny in two species of cichlids: an SEM study. J Morphol 1989, 202:53-68.
• [45]Konings A: Ad Koning’s Book of Cichilds and Other Fishes of Lake Malawi. Neptune City, NJ: TFH Publications; 1990.
• [46]Konings A: Malawi Cichlids in their Natural Habitat. 4th edition. El Paso, TX: Cichlid Press; 2007.
• [47]Webb JF, Bird NC, Carter L, Dickson J: Comparative development and evolution of two lateral line phenotypes in Lake Malawi cichlids. J Morphol 2014, 275:678-692.
• [48]Schwalbe MAB, Webb JF: The effect of light intensity on prey detection behavior in two Lake Malawi cichlids, Aulonocara stuartgranti and Tramitichromis sp. J Comp Physiol A,in press
• [49]Hall BK: The role of movement and tissue interactions in the development and growth of bone and secondary cartilage in the clavicle of the embryonic chick. J Embryol Exp Morph 1986, 93:133-152.
• [50]Potthoff T, Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall AW Jr, Richardson SL, Lawrence KS: Clearing and staining technique. In Ontogeny and Systematics of Fishes. American Society of Ichthyologists and Herpetologists Special Publication No. 1. Lawrence, KS: Allen Press Inc; 1984:35-37.
• [51]Johnson PO, Neyman J: Tests of certain linear hypotheses and their application to some educational problems. Stat Res Mem 1936, 1:57-93.
• [52]White CR: Allometric analysis beyond heterogeneous regression slopes: use of the Johnson-Neyman technique in comparative biology. Physiol Biochem Zool 2003, 76:135-140.
• [53]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, 5:522-531.
• [54]Klingenberg CP: Morphological integration and developmental modularity. Ann Rev Ecol Evol Syst 2008, 39:115-132.
• [55]Klingenberg CP: Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 2010, 11:623-635.
• [56]Raff EC, Raff RA: Dissociability, modularity, evolvability. Evol Dev 2000, 2:235-237.
• [57]Polly PD, Head JJ, Cohn MJ: Testing modularity and dissociation: the evolution of regional proportions in snakes. In Beyond Heterochrony: the Evolution of Development. Edited by Zelditch ML. New York: Wiley-Liss, Inc; 2001:305-335.
• [58]Becker EA: The distribution and ontogeny of neuromast receptor organs and a comparison of methods for chemical ablation of the lateral line system in two cichlid fishes. Master’s thesis: University of Rhode Island, Department of Biological Sciences; 2013.
• [59]Montgomery JC, Bleckmann H, Coombs S: Sensory ecology and neuroethology of the lateral line. In The Lateral Line System. Edited by Coombs S, Bleckmann H, Fay RR, Popper AN. New York: Springer; 2014:121-150.
• [60]DeBeer GR: The Development of the Vertebrate Skull. Chicago: University of Chicago Press; 1985.
• [61]Graham-Smith W: On the lateral lines and dermal bones in the parietal region of some crossopterygian and dipnoan fishes. Phil Trans R Soc Lond 1978, 282:41-105.
• [62]Patterson C: Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the endoskeleton. In Problems in Vertebrate Evolution. Edited by Andrews SM, Miles RS, Walker AD. New York: Academic; 1977:77-121.
• [63]Schaeffer B: The dermal skeleton of fishes. In Problems in Vertebrate Evolution. Edited by Andrews SM, Miles RS, Walker AD. New York: Academic; 1977:25-52.
• [64]Atchley WR, Hall BK: A model for development and evolution of complex morphological structures. Biol Rev 1991, 66:101-157.
• [65]Schlosser G: The role of modules in development and evolution. In Modularity in Development and Evolution. Edited by Schlosser G, Wagner GP. Chicago: The University of Chicago Press; 2004:519-582.
• [66]Goswami A, Weisbecker V, Sanchez-Villagra MR: Developmental modularity and the marsupial-placental dichotomy. J Exp Zool (Mol Dev Evol) 2009, 312B:186-195.
• [67]Koyabu D, Werneburg I, Morimoto N, Zollikofer CP, Forasiepi AM, Endo H, Kimura J, Ohdachi SD, Truong Son N, Sánchez-Villagra MR: Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size. Nat Commun 2014, 5:3625.
• [68]McNamara KJ: Heterochrony: the evolution of development. Evol Edu Outreach 2012, 5:203-218.
• [69]Hulsey CD, Fraser GJ, Streelman JT: Evolution and development of complex biomechanical systems: 300 million years of fish jaws. Zebrafish 2005, 2:243-257.
• [70]Asaoka A, Nakae M, Sasaki K: Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobiods (Perciformes: Rhyacichthyidae). Icthyol Res 2014, 61:49-58.
• [71]Gregory WK: Fish skulls: a study of the evolution of natural mechanisms. Trans Am Phil Soc 1933., 23i-vii+75-481
• [72]Monteiro LR, Bonato V, dos Reis SF: Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evol Dev 2005, 7:429-439.
• [73]Zelditch ML, Wood AR, Bonett RM, Swiderski DL: Modularity of the rodent mandible: integrating bones, muscles, and teeth. Evol Dev 2008, 10:756-768.
• [74]Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, Fisher S: Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE 2012, 7:e47394.
• [75]Fujimura K, Okada N: Bone development in the jaw of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Dev Growth Differ 2008, 50:339-355.
• [76]Parsons KJ, Marquez E, Albertson RC: Constraint and opportunity: the genetic basis and evolution of modularity in the cichlid mandible. Am Nat 2012, 179:64-78.
• [77]Wagner GP: Homologues, natural kinds and the evolution of modularity. Am Zool 1996, 36:36-43.
• [78]Reno HW: The lateral-line system of the silverjaw minnow, Ericymba buccata Cope. Southwest Nat 1971, 15:347-358.
• [79]McDonnell R: On the system of the “lateral line” in fishes. Trans R Irish Acad Sci 1871, 24:161-188.
• [80]Sakamoto K: Interrelationships of the family Pleuronectidae (Pisces: Pleuronectiformes). Mem Fac Fish, Hokkaido Univ 1984, 31:95-215.
• [81]Webb JF: Lateral Line Structure. In Encyclopedia of Fish Physiology: from Genome to Environment. Edited by Farrell AP. San Diego: Academic; 2011:336-346. [Volume 1]
• [82]Disler NN: Lateral Line Sense Organs and their Importance in Fish Behavior. Israel Program for Scientific Translations: Jerusalem; 1971.
• [83]Ćurčić-Blake B, van Netten SM: Source location encoding in the fish lateral line canal. J Exp Biol 2006, 209:1548-1559.