Developmental plasticity and the evolution of animal complex life cycles

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1540, 2010, Pages 631-640

  Minelli, Alessandro ^a   Fusco, Giuseppe ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Comparative analysis; Larvae; Life cycle evolution; Metamorphosis; Polyphenism

Indexed keywords

COMPARATIVE STUDY; ENVIRONMENTAL CONDITIONS; EVOLUTIONARY BIOLOGY; LARVA; METAMORPHOSIS; ONTOGENY; PHENOTYPIC PLASTICITY; POLYMORPHISM; PROTOZOAN; REPRODUCTIVE BEHAVIOR; SPECIES DIVERSITY;

ANIMALIA; METAZOA;

EID: 76749162813     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0268     Document Type: Review

References (101)

1. Anderson, R. C. 1984 The origins of zooparasitic nematodes. Can. J. Zool. 62, 317-328. (doi:10.1139/z84-050)
2. Antebi, A., Culotti, J. G. Hedgecock, E. M. 1998 daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 125, 1191-1205.
3. Antebi, A., Yeh, W. H., Tait, D., Hedgecock, E. M. Riddle, D. L. 2000 daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev. 14, 1512-1527.
4. Appleby, J. H. Credland, P. F. 2007 The role of temperature and larval crowding in morph determination in a tropical beetle, Callosobruchus subinnotatus. J. Insect Physiol. 53, 983-993. (doi:10.1016/j.jinsphys.2007.05. 001) (Pubitemid 47488375)
5. Arbeitman, M. N. et al. 2002 Gene expression during the life cycle of Drosophila melanogaster. Science 297, 2270-2275. (doi:10.1126/science.1072152)
6. Bavestrello, G., Sommer, C. Sarà, M. 1992 Bi-directional conversion in Turritopsis nutricula. Sci. Mar. 56, 137-140.
7. Begun, D. J. Collins, J. P. 1992 Biochemical plasticity in the Arizona tiger salamander (Ambystoma tigrinum nebulosum). J. Hered. 83, 224-227.
8. Bell, G. Mooers, A. O. 1997 Size and complexity among multicellular organisms. Biol. J. Linn. Soc. 60, 345-363. (doi:10.1111/j.1095-8312.1997. tb01500.x)
9. Berlese, A. 1913 Intorno alle metamorfosi degli insetti. Redia 9, 121-136.
10. Bologna, M. A. Pinto, J. P. 2001 Phylogenetic studies of the Meloidae (Coleoptera), with emphasis on the evolution of phoresy. Syst. Entom. 26, 33-72. (doi:10.1046/j.1365-3113.2001.00132.x) (Pubitemid 32100642)
11. Bologna, M. A., Oliverio, M., Pitzalis, M. Mariottini, P. 2008 Phylogeny and evolutionary history of the blister beetles (Coleoptera, Meloidae). Mol. Phylogenet. Evol. 48, 679-693. (doi:10.1016/j.ympev.2008.04.019)
12. Bonner, J. T. 1988 The evolution of complexity by means of natural selection. Princeton, NJ: Princeton University Press.
13. Braendle, C., Caillaud, M. C. Stern, D. L. 2005a Genetic mapping of aphicarus-a sex-linked locus controlling a wing polymorphism in the pea aphid (Acyrthosiphon pisum). Heredity 94, 435-442. (doi:10.1038/sj.hdy.6800633)
14. Braendle, C., Friebe, I., Caillaud, M. C. Stern, D. L. 2005b Genetic variation for an aphid polyphenism is genetically linked to a naturally occurring wing polymorphism. Proc. R. Soc. B 272, 657-664. (doi:10.1098/rspb. 2004.2995) (Pubitemid 41411148)
15. Brisson, J. 2010 Aphid wing dimorphism: linking environmental and genetic control of trait variation. Phil. Trans. R. Soc. B 365, 605-616. (doi:10.1098/rstb.2009.0255)
16. Cassada, R. C. Russell, R. L. 1975 The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev. Biol. 46, 326-342. (doi:10.1016/0012-1606(75)90109-8)
17. Chia, F.-S., Gibson, G. Qian, Y. 1996 Poecilogony as a reproductive strategy of marine invertebrates. Oceanol. Acta 19, 203-208.
18. Cowen, L. E. Lindquist, S. 2005 Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309, 2185-2189. (doi:10.1126/science.1118370) (Pubitemid 41396062)
19. Dworkin, I. 2005a Canalization, cryptic variation, and developmental buffering: a critical examination and analytical perspective. In Variation-a central concept in biology (eds B. Hallgrímsson B. K. Hall), pp. 131-158. Amsterdam, The Netherlands/New York: Elsevier/ Academic Press.
20. Dworkin, I. 2005b Towards a genetic architecture of cryptic genetic variation and genetic assimilation: the contribution of K.G. Bateman. J. Genet. 84, 223-226. (doi:10.1007/BF02715794)
21. Félix, A. 2005 An inversion in wiring of an intercellular signal: evolution of Wnt signaling in the nematode vulva. BioEssays 27, 765-769. (doi:10.1002/bies.20275) (Pubitemid 41297398)
22. Fenton, A., Paterson, S., Viney, M. E. Gardner, M. P. 2004 Determining the optimal developmental route of Strongyloides ratti: an evolutionarily stable strategy approach. Evolution 58, 989-1000.
23. Ferrari, F. D. Dahms, U. 2007 Post-embryonic development of the Copepoda. Leiden, The Netherlands: Brill Academic.
24. Fryer, G. 1961 The developmental history of Mutela bourguignati (Ancey) Bourguignat (Mollusca: Bivalvia). Phil. Trans. R. Soc. Lond. B 244, 259-298. (doi:10.1098/rstb.1961.0009)
25. Fusco, G. Minelli, A. 2000 Measuring morphological complexity of segmented animals: centipedes as model systems. J. Evol. Biol. 13, 38-46. (doi:10.1046/j.1420-9101.2000.00139.x) (Pubitemid 30065057)
26. Futahashi, R. Fujiwara, H. 2008 Identification of stagespecific larval camouflage associated genes in the swallowtail butterfly Papilio xuthus. Dev. Genes Evol. 218, 491-504. (doi:10.1007/s00427-008-0243-y)
27. Galaktionov, K. V. Dobrovolskij, A. A. 2003 The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, and evolution of digenetic trematodes. Dordrecht, The Netherlands: Kluwer Academic.
28. Garstang, W. 1922 The theory of recapitulation: a critical restatement of the biogenetic law. J. Linn. Soc. Zool. 35, 81-101. (doi:10.1111/j.1096-3642. 1922.tb00464.x)
29. Giard, A. 1905 La poecilogonie. C. R. VI Congr. Int. Zool., Berne 1904, pp. 617-646.
30. Gibson, G. D. Chia, S. 1989 Developmental variability (benthic and pelagic) in Haminaea callidigenita (Opisthobranchia: Cephalaspidea) is influenced by egg mass jelly. Biol. Bull. 176, 103-110. (doi:10.2307/1541577)
31. Giroux, S. Corey, E. J. 2007 Stereocontrolled synthesis of dafachronic acid A, the ligand for the DAF-12 nuclear receptor of Caenorhabditis elegans. J. Am. Chem. Soc. 129, 9866-9867. (doi:10.1021/ja074306i) (Pubitemid 47257772)
32. Glenner, H. Høeg, J. T. 1995 A new motile, multicellular stage involved in host invasion by parasitic barnacles (Rhizocephala). Nature 377, 147-150. (doi:10.1038/377147a0) (Pubitemid 26448751)
33. Gould, S. J. 1977 Ontogeny and phylogeny. Cambridge, MA: Belknap Press.
34. Greene, E. 1999 Phenotypic variation in larval development and evolution: polymorphism, polyphenism, and developmental reaction norms. In The origin and evolution of larval forms (eds B. K. Hall M. H. Wake), pp. 379-410.San Diego, CA: Academic Press.
35. Hadfield, M. G. Pennington, J. T. 1990 Nature of the metamorphic signal and its internal transduction in larvae of the nudibranch Phestilla sibogae. Bull. Mar. Sci. 46, 455-464.
36. Hadfield, M. G., Carpizo-Ituarte, E. J., del Carmen, K. Nedved, B. T. 2001 Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am. Zool. 41, 1123-1131. (doi:10.1668/0003-1569(2001)041[1123:MCAMAC]2. 0.CO;2)
37. Haeckel, E. 1866 Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformirte Descendenz-Theorie. Band 1: Allgemeine Anatomie der Organismen. Berlin, Germany: Georg Reimer.
38. Hall, B. K. 1998 Evolutionary developmental biology, 2nd edn. London, UK: Chapman Hall.
39. Heming, B. S. 2003 Insect development and evolution. Ithaca/ New York: Comstock Publishing Associates/Cornell University Press.
40. Holt, S. J. 2006 Staying alive in adversity: transcriptome dynamics in the stress-resistant dauer larva. Funct. Integr. Genomics 6, 285-299. (doi:10.1007/s10142-006-0024-5) (Pubitemid 44263937)
41. Hughes, N. C., Minelli, A. Fusco, G. 2006 The ontogeny of trilobite segmentation: a comparative approach. Paleobiology 32, 603-628. (doi:10.1666/06017.1) (Pubitemid 44873479)
42. Inestrosa, N. C., Gonzalez, M. Campos, E. O. 1993 Metamorphosis of Concholepas concholepas (Bruguière, 1789) induced by excess potassium. J. Shell Res. 12, 337-341.
43. Jablonski, D. 2005 Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. J. Exp. Zool. B 304, 504-519.
44. Jackson, D., Leys, S. P., Hinman, V. F., Woods, R., Levin, M. F. Degnan, B. M. 2002 Ecological regulation of development: induction of marine invertebrate metamorphosis. Int. J. Dev. Biol. 46, 679-686.
45. Jacobs, M. W., Degnan, B. M., Bishop, J. D. D. Strathmann, R. R. 2008 Early activation of adult organ differentiation during delay of metamorphosis in solitary ascidians, and consequences for juvenile growth. Invert. Biol. 127, 217-236. (doi:10.1111/j.1744-7410.2008.00125.x) (Pubitemid 351748732)
46. Kenyon, C. J. et al. 1997 The dance of the Hox genes: patterning the anteroposterior axis of Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 62, 293-305. (doi:10.1101/SQB.1997.062.01.036)
47. Koutsos, A. C. et al. 2007 Life cycle transcriptome of the malaria mosquito Anopheles gambiae and comparison with the fruitfly Drosophila melanogaster. Proc. Natl Acad. Sci. USA 104, 11 304-11 309. (doi:10.1073/pnas. 0703988104) (Pubitemid 47175136)
48. Krug, P. J. 1998 Poecilogony in an estuarine opisthobranch: planktotrophy, lecitotrophy, and mixed clutches in a population of the ascoglossan Alderia modesta. Mar. Biol. 132, 483-494. (doi:10.1007/ s002270050414) (Pubitemid 28533914)
49. Larink, O. Westheide, W. 2006 Coastal plankton. Photo guide for European seas. München, Germany: Pfeil.
50. Larsen, K. 2001 Morphological and molecular investigation of polymorphism and cryptic species in tanaid crustaceans: implications for tanaid systematics and biodiversity estimates. Zool. J. Linn. Soc. 131, 353-379. (doi:10.1111/j.1096-3642.2001.tb02241.x)
51. Larsen, K. 2005 Deep-sea Tanaidacea (Peracarida) from the Gulf of Mexico. Leiden, The Netherlands: Brill.
52. Lemaire, P. 2009 Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. Dev. Biol. 332, 48-60. (doi:10.1016/j.ydbio.2009.05. 540)
53. Love, A. 2010 Idealization in evolutionary developmental investigation: a tension between plasticity and normal stages. Phil. Trans. R. Soc. B 365, 679-690. (doi:10.1098/rstb.2009.0262)
54. Manni, L. Burighel, P. 2006 Common and divergent pathways in alternative developmental processes of ascidians. BioEssays 28, 902-912. (doi:10.1002/bies.20462) (Pubitemid 44433753)
55. Marsh, A. G. Fielman, K. T. 2005 Transcriptome profiling of individual larvae of two different developmental modes in the poecilogonous polychaete Streblospio benedicti (Spionidae). J. Exp. Zool. B 304, 238-249.
56. McKinney, M. L. McNamara, K. J. 1991 Heterochrony. The evolution of ontogeny. New York, NY: Plenum Press.
57. McNamara, K. J. (ed.) 1995 Evolutionary change and heterochrony. Chichester, UK: John Wiley Sons.
58. McShea, D. W. 1991 Complexity and evolution: what everybody knows. Biol. Philos. 6, 303-324. (doi:10.1007/BF00132234)
59. McShea, D. W. 1992 A metric for the study of evolutionary trends in the complexity of serial structures. Biol. J. Linn. Soc. 45, 39-55. (doi:10.1111/j.1095-8312.1992.tb00630.x)
60. McShea, D. W. 1996a Complexity and homoplasy. In Homoplasy: the recurrence of similarity in evolution (ed. M. J. Sanderson L. Hufford), pp. 207-225. San Diego, CA: Academic Press.
61. McShea, D. W. 1996b Metazoan complexity and evolution: s there a trend? Evolution 50, 477-492. (doi:10.2307/2410824)
62. McShea, D. W. 2000 Functional complexity in organisms: parts as proxies. Biol. Philos. 15, 641-668. (doi:10.1023/A:1006695908715) (Pubitemid 32046443)
63. Mikhailov, K. V. et al. 2009 The origin of Metazoa: a transition from temporal to spatial cell differentiation. BioEssays 31, 758-768. (doi:10.1002/bies.200800214)
64. Minelli, A. 2003 The development of animal form: ontogeny, morphology, and evolution. Cambridge, UK: Cambridge University Press.
65. Minelli, A. 2009 Perspectives on animal phylogeny and evolution. Oxford, UK: Oxford University Press.
66. Minelli, A., Brena, C., Deflorian, G., Maruzzo, D. Fusco, G. 2006 From embryo to adult-beyond the conventional periodization of arthropod development. Dev. Genes Evol. 216, 373-383. (doi:10.1007/s00427-006-0075-6) (Pubitemid 44057482)
67. Moczek, A. P. 2007 Developmental capacitance, genetic accommodation, and adaptive evolution. Evol. Dev. 9, 299-305.
68. Moczek, A. 2010 Phenotypic plasticity and diversity in insects. Phil. Trans. R. Soc. B 365, 593-603. (doi:10.1098/rstb.2009.0263)
69. Motola, D. L. et al. 2006 Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124, 1209-1223. (doi:10.1016/j.cell.2006.01.037)
70. Nijhout, H. F. 1994 Insect hormones. Princeton, NJ: Princeton University Press.
71. Nijhout, H. F. 1999 Hormonal control in larval development and evolution. In The origin and evolution of larval forms (eds M. Wake B. Hall), pp. 217-254. New York, NY: Academic Press.
72. Nijhout, H. F. 2003 Development and evolution of adaptive polyphenism. Evol. Dev. 5, 9-18. (doi:10.1046/j.1525-142X.2003.03003.x) (Pubitemid 36174972)
73. Nijhout, H. F., Dawidowitz, J. Roff, D. 2006 A quantitative analysis of the mechanism that controls body size in Manduca sexta. J. Biol. 5, 16. (doi:10.1186/jbiol43) (Pubitemid 46251349)
74. Nikolei, E. 1961 Vergleichende Untersuchungen zur Fortpflanzung der heterogenen Gallmücken unter experimentellen Bedingungen. Ztschr. Morphol. Ö kol. Tiere 50, 281-329. (doi:10.1007/BF00389719)
75. Noor, M. A. F., Parnell, R. S. Grant, B. S. 2008 A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars. PLoS ONE 3, e3142. (doi:10.1371/journal.pone.0003142)
76. Ogawa, A., Streit, A., Antebi, A. Sommer, R. J. 2009 A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Curr. Biol. 19, 67-71. (doi:10.1016/j.cub.2008.11.063)
77. Omodeo, P., Minelli, A. Baccetti, B. 1980 On the phylogeny of pterygote insects. Boll. Zool. 47(Suppl.), 49-63.
78. Pechenik, J. A. Eyster, L. S. 1989 Influence of delayed metamorphosis on the growth and metabolism of young Crepidula fornicata (Gastropoda) juveniles. Biol. Bull. 176, 14-24. (doi:10.2307/1541884)
79. Piraino, S., Boero, F., Aeschbach, B. Schmid, V. 1996 Reversing the life cycle: medusae transforming into polyps and cell transdifferentiation in Turritopsis nutricula (Cnidaria, Hydrozoa). Biol. Bull. 190, 302-312. (doi:10.2307/1543022)
80. Pollock, D. A. Normark, B. B. 2002 The life cycle of Micromalthus debilis LeConte (1878) (Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. J. Zool. Syst. Evol. Res. 40, 105-112. (doi:10.1046/j.1439-0469.2002.00183.x) (Pubitemid 34689294)
81. Poulin, R. 2007 Evolutionary ecology of parasites, 2nd edn. Princeton, NJ: Princeton University Press.
82. Queitsch, C., Sangster, T. A. Lindquist, S. 2002 Hsp90 as a capacitor of phenotypic variation. Nature 417, 618-624. (doi:10.1038/nature749) (Pubitemid 34614814)
83. Raff, R. A. Wray, G. A. 1989 Heterochrony: developmental mechanisms and evolutionary results. J. Evol. Biol. 2, 409-434. (doi:10.1046/j.1420-9101.1989. 2060409.x)
84. Rutherford, S. L. Lindquist, S. 1998 Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342. (doi:10.1038/24550) (Pubitemid 28557387)
85. Saunders, P. T. Ho, M. V. 1984 The complexity of organisms. In Evolutionary theory: paths into the future (ed. J. W. Pollard), pp. 121-139. Chichester, UK: Wiley.
86. Schlichting, C. 2003 Origins of differentiation via phenotypic plasticity. Evol. Dev. 5, 98-105. (doi:10.1046/j.1525-142X.2003.03015.x) (Pubitemid 36174984)
87. Schlichting, C. D. Pigliucci, M. 1998 Phenotypic evolution: a reaction norm perspective. Sunderland, MA: Sinauer.
88. Schmidt, A., Siegel, V. Brandt, A. 2002 Postembryonic development of Apseudes heroae and Allotanais hirsutus (Tanaidacea, Crustacea) in Magellanic and sub-Antarctic waters. Antarct. Sci. 14, 201-211. (doi:10.1017/ S0954102002000019) (Pubitemid 34979151)
89. Sieg, J. 1978 Bemerkungen zur Möglichkeit der Bestimmung der Weibchen bei den Dikonophora and der Entwicklung der Tanaidaceen. Zool. Anz. 200, 233-241.
90. Snow, M. I. Larsen, P. L. 2000 Structure and expression of daf-12: a nuclear hormone receptor with three isoforms that are involved in development and aging in Caenorhabditis elegans. Biochim. Biophys. Acta 1494, 104-116.
91. Stoner, A. W., Ray, M., Glazer, R. A. Mccarthy, E. J. 1996 Metamorphic responses to natural substrates in a gastropod larva: decisions related to postlarval growth and habitat preference. J. Exp. Mar. Biol. Ecol. 205, 229-249. (doi:10.1016/S0022-0981(96) 02614-7)
92. Suzuki, Y. Nijhout, H. F. 2006 Evolution of a polyphenism by genetic accommodation. Science 311, 650-652. (doi:10.1126/science.1118888) (Pubitemid 43191307)
93. Taylor, J. J., Southgate, P. C. Rose, R. A. 1998 Assessment of artificial substrates for collection of hatchery-reared silver-slip oyster (Pinctada maxima Jameson) spat. Proc. Natl Acad. Sci. USA 83, 7658-7662.
94. Truman, J. W. Riddiford, L. M. 1999 The origins of insect metamorphosis. Nature 401, 447-452. (doi:10.1038/46737) (Pubitemid 29470196)
95. Valentine, J. W. 2004 On the origin of phyla. Chicago, IL: University of Chicago Press.
96. Vowels, J. J. Thomas, J. H. 1992 Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105-123.
97. West-Eberhard, M. J. 2003 Developmental plasticity and evolution. New York, NY: Oxford University Press.
98. Wiegmann, B. M., Trautwein, M. D., Kim, J.-W., Cassel, B. K., Bertone, M. A., Winterton, S. L. Yeates, D. K. 2009 Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 7, 34. (doi:10.1186/1741- 7007-7-34)
99. Wyatt, I. J. 1961 Pupal paedogenesis in the Cecidomyidae (Diptera) I. Proc. R. Entom. Soc. A 36, 133-143.
100. Wyatt, I. J. 1964 Immature stages of Lestremiinae (Diptera: Cecidomyidae) infesting cultivated mushrooms. Trans. R. Entom. Soc. Lond. 116, 15-27.
101. Zakhvatkin, Y. A. 1949 The comparative embryology of the low invertebrates. Sources and method of the origin of metazoan development. Moscow, Russia: Soviet Science.