Can heterochrony help explain the high morphological diversity within the genus Niphargus (Crustacea: Amphipoda)?

Organisms Diversity and Evolution

Volumn 8, Issue 2, 2008, Pages 146-162

  Fišer, Cene ^a   Bininda Emonds, Olaf R P ^b   Blejec, Andrej ^a,c   Sket, Boris ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

Author keywords

'Cryptic' speciation; Heterochrony; Niphargus; Phenotypic diversity; Postembryonic development

Indexed keywords

ALLOMETRY; AMPHIPOD; CRYPSIS; DIACHRONISM; EMBRYONIC DEVELOPMENT; EVOLUTION; GROWTH RATE; MORPHOLOGY; SEXUAL DIMORPHISM; SPECIATION (BIOLOGY);

AMPHIPODA; CRUSTACEA; NIPHARGUS;

EID: 43049136651     PISSN: 14396092     EISSN: 16181077     Source Type: Journal    
DOI: 10.1016/j.ode.2007.06.002     Document Type: Article

References (79)

1. Aden E. Adaptation to darkness. In: Culver D.C., and White W.B. (Eds). Encyclopaedia of Caves (2005), Elsevier Academic Press, Oxford 1-3
2. Alberch P. Problems with interpretation of developmental sequences. Syst. Zool. 34 (1985) 46-58
3. Alberch P., Gould S.J., Oster G.F., and Wake D.B. Size and shape in ontogeny and phylogeny. Paleobiology 5 (1979) 296-317
4. Barnard J.L., and Barnard C.M. Freshwater Amphipoda of the World, I. Evolutionary Patterns (1983), Hayfield Associates, Mt. Vernon, Virginia pp. 156-161
5. Bat L., Akbulut M., Sezgin M., and Çulha M. On the occurrence of Niphargus valachicus Dobrenau & Manolache, 1933 (Amphipoda, Gammaridae) in the Western Black Sea Region of Turkey. Turk. J. Zool. 25 (2000) 235-239
6. Bininda-Emonds O.R.P., Jeffery J.E., Coates M.I., and Richardson M.K. From Haeckel to event-pairing: the evolution of developmental sequences. Theor. Biosci. 121 (2002) 297-320
7. Bininda-Emonds O.R.P., Jeffery J.E., and Richardson M.K. Is sequence heterochrony an important evolutionary mechanism in mammals?. J. Mamm. Evol. 10 (2003) 335-361
8. Bininda-Emonds O.R.P., Jeffery J.E., and Richardson M.K. Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proc. R. Soc. Lond. B 270 (2003) 341-346
9. Chapelle G. Estimating size of amphipods in life cycle studies: what to measure and what for?. Pol. Arch. Hydrobiol. 42 (1995) 295-302
10. Christiansen K. Morphological adaptations. In: Culver D.C., and White W.B. (Eds). Encyclopaedia of Caves (2005), Elsevier Academic Press, Oxford 386-397
11. Denöel M., and Schabetsberger R. Resource partitioning in two heterochronic populations of Greek Alpine newts, Triturus alpinus veluchiensis. Acta Oecol. 24 (2003) 55-64
12. Fišer C., Sket B., and Trontelj P. The taxonomic complexity of the genus Niphargus (Crustacea: Amphipoda) and an approach to its elucidation. In: Latella L., Mezzanotte E., and Tarroco M. (Eds). XVI International Symposium of Biospeleology, 8-15 September 2002 (2002), Museo Civico di Storia Naturale di Verona, Verona, Italy 39-40
13. Fišer C., Trontelj P., and Sket B. Phylogenetic analysis of the Niphargus orcinus species aggregate (Crustacea: Amphipoda: Niphargidae) with description of new taxa. J. Nat. Hist. 40 41-43 (2006) 2265-2315
14. Fišer C., Sket B., and Stoch F. Distribution of four narrowly endemic Niphargus species (Crustacea: Amphipoda) in the Western Dinaric region with description of a new species. Zool. Anz. 245 (2006) 77-94
15. Gilbert S.F., and Bolker J.A. Homologies of processes and modular elements of embryonic construction. In: Wagner G.P. (Ed). The Character Concept in Evolutionary Biology (2001), Academic Press, San Diego 437-456
16. Ginet R. Écologie, éthologie et biologie de Niphargus. Sommaire général. Annls. Spéléol. 15 (1960) 127-237
17. Ginet R. Écologie, éthologie et biologie de Niphargus. Cycle biologique de Niphargus. Annls. Spéléol. 15 (1960) 239-376
18. Gould S.J. Ontogeny and Phylogeny (1977), Belknap Press, Cambridge, MA
19. Gould S.J. Of coiled oysters and big brains: how to rescue the terminology of heterochrony now gone astray. Evol. Dev. 2 (2000) 241-248
20. Jeffery J.E., Richardson M.K., Coates M.I., and Bininda-Emonds O.R.P. Analyzing developmental sequences within a phylogenetic framework. Syst. Biol. 51 (2002) 478-491
21. Jeffery J.E., Bininda-Emonds O.R.P., Coates M.I., and Richardson M.K. Analyzing evolutionary patterns in amniote embryonic development. Evol. Dev. 4 (2002) 292-302
22. Jeffery J.E., Bininda-Emonds O.R.P., Coates M.I., and Richardson M.K. A new technique for identifying sequence heterochrony. Syst. Biol. 54 (2005) 230-240
23. Jersche G. Zur Artfrage und Variabilität von Niphargus tatrensis Wrzesnowski (Ein Beitrag zur postembryonalen Veränderung taxonomischer Merkmale). Z. Zool. Syst. Evol. Forschg. 1 (1963) 240-276
24. Karaman S. Die unterirdischen Amphipoden Südserbiens. Ohridski Zbornik 34 (1943) 163-313
25. Karaman S. Podrod Orniphargus u Jugoslaviji I-II. O nekim amfipodima-izopodima Balkana i o njihovoj sistematici. Srpska Akad. Nauka - Posebna Izdanja 163 (1950) 119-159
26. Karaman G. First discovery of genus Niphargus Sch. in Iraq, Israel and adjacent regions, with description of N. itus, new species (fam. Niphargidae) (Contribution to the knowledge of the Amphipoda 153). Poljepriv. Šumarstvo 32 (1986) 13-36
27. Karaman G. New species of family Niphargidae and new localities of some other subterranean Gamaridean species from Yugoslavia (Contribution to the knowledge of the Amphipoda 166). Glas. Repub. Zavoda Zašt. Prir. Prir. Muz. Titogr. 19 (1989) 15-32
28. Karaman G. Fam. Niphargidae. In: Karaman G. (Ed). Crustacea Amphipoda di aqua dolce, Fauna d'Italia (1993), Edizioni Calderini, Bologna 157-284
29. Karaman G. First discovery of the family Niphargidae (Gammaridea) in Iran. Glas. Od. Prirod. Nauk. - Crnog. Akad. Nauka Umet. 12 (1998) 9-22
30. Karaman G. New data on some gammaridean amphipods (Amphipoda, Gammaridea) from Palearctic. Glas. Od. Prirod. Nauk. - Crnog. Akad. Nauka Umet. 15 (2003) 21-39
31. Karaman G., and Ruffo S. Amphipoda: Niphargus-group (Niphargidae sensu Bousfield, 1982). In: Botosaneanu L. (Ed). Stygofauna Mundi (1986), Backhuys & Brill, Leiden 514-534
32. Klingenberg C.P. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol. Rev. 73 (1998) 79-123
33. Kluge A.G. Ontogeny and phylogenetic systematics. Cladistics 1 (1985) 13-27
34. Koenemann S., and Schram F.R. The limitations of ontogenetic data in phylogenetic analyses. Bijdr. Dierdk. 71 (2002) 47-65
35. Kokkotis A.T., and McLaughlin J.D. Instar-specific head and body lengths of Hyalella (Amphipoda): criteria for starting and endpoints in experimental studies. Hydrobiologia 474 (2002) 223-227
36. Langecker T.G. The effects of continuous darkness on cave ecology and cavernicolous evolution. In: Wilkens H., Culver D.C., and Humphreys W.F. (Eds). Ecosystems of the World 30: Subterranean Ecosystems (2000), Elsevier Press, Amsterdam 135-157
37. Lefébure T., Douady C.J., Gouy M., Trontelj P., Briolay J., and Gibert J. Molecular phylogeography of Niphargus virei. Mol. Ecol. 15 (2006) 1797-1806
38. Mabee P.M., and Trendler T.A. Development of the cranium and paired fins in Betta splendens (Teleostei: Percomorpha): intraspecific variation and interspecific comparisons. J. Morphol. 227 (1996) 249-287
39. Mabee P.M., Olmstead K.L., and Cubbage C.C. An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54 (2000) 2091-2106
40. Marques A.C., and Gnaspini P. The problem of characters susceptible to parallel evolution in phylogenetic reconstructions: suggestion of a practical method and its application to cave animals. Cladistics 17 (2001) 371-381
41. Mathieu J., Jeannerod F., Hervant F., and Kane T.C. Genetic differentiation of Niphargus rhenorhodanensis (Amphipoda) from interstitial and karst environments. Aquat. Sci. 59 (1997) 39-47
42. McNamara K.J. Sexual dimorphism: the role of heterochrony. In: McNamara K.J. (Ed). Evolutionary change and heterochrony (1995), Wiley, Chichester 65-89
43. Minelli A., and Fusco G. Body segmentation and segment differentiation: the scope for heterochronic change. In: McNamara K.J. (Ed). Evolutionary change and heterochrony (1995), Wiley, Chichester 49-63
44. Morand C. Contribution a l'étude taxonomique de Niphargus: note préliminaire a l'étude de la croissance comparée de 2 populations de Niphargus longicaudatus rhenorhodanensis (Amphipodes, Gammaridea). Crustaceana 27 (1974) 249-254
45. Nelson G. Ontogeny, phylogeny, paleontology and biogenetic law. Syst. Zool. 27 (1978) 324-345
46. Nijhout F.H. Insect hormones (1994), Princeton University Press, Princeton, NJ
47. Nunn C.L., and Smith K.K. Statistical analyses of developmental sequences: the craniofacial region in marsupial and placental mammals. Am. Nat. 152 (1998) 82-101
48. Pinkster S. Amphipoda. In: Illies J. (Ed). Limofauna Europaea (1978), Gustav Fischer Verlag, Stuttgart 244-253
49. Prevorčnik S., Blejec A., and Sket B. Racial differentiation in Asellus aquaticus (L.) (Crustacea: Isopoda: Asellidae). Arch. Hydrobiol. 160 (2004) 193-214
50. Proudlove G.S., Wood P.J., Harding P.T., Horne D.J., and Knight L.R.F.D. A review of the status and distribution of the subterranean aquatic Crustacea of Britain and Ireland. Cave Karst Sci. 30 (2003) 53-74
51. Reilly S.M., Wiley E.O., and Meinhardt D.J. An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol. J. Linn. Soc. 60 (1997) 119-143
52. Richardson M.K., and Keuck G. Haeckel's ABC of evolution and development. Biol. Rev. 77 (2002) 495-528
53. Richardson M.K., and Oelschläger H.H.A. Time, pattern and heterochrony: a study of hyperphalangy in the dolphin embryo flipper. Evol. Dev. 4 (2002) 435-444
54. Richardson M.K., Jeffery J.E., Coates M.I., and Bininda-Emonds O.R.P. Comparative methods in developmental biology. Zoology 104 (2001) 278-283
55. Ruffo, S., 1953a. Lo stato attuale delle conoscenze sulla distribuzione geographica degli Anfipodi delle acque sotteranee europee e dei paesi mediterranei. In: Premier Congres International de Spéléologie, pp. 13-37.
56. Ruffo S. Studi sui Crostacei Anfipodi XXXVIII. Nuovi Niphargus (Amphipoda Gammaridae) della Venezia Tridentina. Studi Trent. Sci. Nat. 30 (1953) 115-127
57. Schlosser G. Using heterochrony plots to detect the dissociated coevolution of characters. J. Exp. Zool. (Mol. Dev. Evol.) 291 (2001) 282-304
58. Schulmeister S., and Wheeler W.C. Comparative and phylogenetic analysis of developmental sequences. Evol. Dev. 6 (2004) 50-57
59. Sket B. Die Niphargus jovanovici-Gruppe (Amphipoda, Gammaridae) in Jugoslawien und NO-Italien, taxonomisch, zoogeographisch und phylogenetisch betrachtet. Razpr. Slov. Akad. Znan. Umet., Razr. Naravosl. Vede 15 (1972) 99-140
60. Sket B. Niphargus stygius (Schiödte) (Amphipoda, Gammaridae) - die Neubeschreibung des Generotypus, Variabilität, Verbreitung und Biologie der Art, I. Biol. Vestn. 22 (1974) 91-103
61. Sket B. Distribution, ecological character, and phylogenetic importance of Niphargus valachicus. Biol. Vestn. 29 (1981) 87-103
62. Sket B. High biodiversity in hypogean waters and its endangerment - the situation in Slovenia, the Dinaric karst, and Europe. Crustaceana 72 (1999) 767-779
63. Sket B. The nature of biodiversity in hypogean waters and how it is endangered. Biodiv. Conserv. 8 (1999) 1319-1338
64. Sket B. Životinjski svijet Vjetrenice (Cave fauna: the particular case of Vjetrenica). In: Lučić I. (Ed). Vjetrenica: Pogled u Dušu Zemlje (Vjetrenica: a glimpse into the soul of the Earth) (2003), Zagreb, ArTresor 147-248
65. Sket B., and Notenboom J. Phylogeny and biogeography of the Niphargus transitvus group of species (Crustacea, Amphipoda). Bijdr. Dierk. 63 (1993) 149-161
66. Sket B., Kaloust P., and Trontelj P. A census of the obligate subterranean fauna of the Balkan Peninsula. In: Griffiths H., Kryštufek B., and Reed J.M. (Eds). Balkan biodiversity (2004), Kluwer Academic, Dordrecht and London 309-322
67. Smirthwaite J.J., Rundle S.D., Bininda-Emonds O.R.P., and Spicer J.I. An integrative approach identifies developmental sequence heterochronies in freshwater basommatophoran snails. Evol. Dev. 9 (2007) 122-130
68. Smith K.K. Comparative patterns of craniofacial development in Eutherian and Metatherian mammals. Evolution 51 (1997) 1663-1678
69. Smith K.K. Heterochrony revisited: the evolution of developmental sequences. Biol. J. Linn. Soc. 73 (2001) 169-186
70. Smith K.K. Sequence heterochrony and the evolution of development. J. Morphol. 252 (2002) 82-97
71. Smith K.K. Time's arrow: heterochrony and the evolution of development. Int. J. Dev. Biol. 47 (2003) 613-621
72. Snedecor G.W., and Cochran W.G. Statistical Methods (1976), Iowa State University Press, Iowa
73. Stoch F. Revision of the Niphargus stygius-group in Venetia and Trentino (northeastern Italy), with description of three new species (Crustacea, Amphipoda, Niphargidae). Boll. Mus. Civ. St. Nat. Verona 22 (1998) 229-274
74. er Colloque Internationale sur le genre Niphargus, Verona, 15-16 Aprile 1969. Museo Civico di Storia Naturale di Verona, pp. 85-90.
75. Trontelj, P., Douday, Ch., Fišer, C., Gibert, J., Gorički, Š., Lefébure, T., Sket, B., Zakšek, V., 2007. A molecular test for cryptic diversity in groundwater: how large are the ranges of macro-stygobionts?. Freshw. Biol. (OnlineEarly), doi:10.1111/j.1365-2427.2007.01877.x.
76. Väinölä R., Witt J.D.S., Grabowski M., Bradbury J.H., Jazdzewski K., and Sket B. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595 (2008) 241-255
77. Velhagen W.A. Analyzing developmental sequences using sequence units. Syst. Biol. 46 (1997) 204-210
78. Verovnik R., Sket B., and Trontelj P. The colonization of Europe by the freshwater crustacean Asellus aquaticus (Crustacea: Isopoda) proceeded from ancient refugia and was directed by habitat connectivity. Mol. Ecol. 14 (2005) 4355-4369
79. Webster M., and Zelditch M.L. Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology 31 (2005) 354-372