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The study of larval tail morphology reveals differentiation between two Triturus species and their hybrids

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In amphibians, morphological differentiation and disparity at the larval and post-metamorphic ontogenetic stages can diverge, owing to various contrasting environments and different selective pressures. In the monophyletic clade of nine Triturus newt species, five different morphotypes can be recognized, but information on larval morphology is limited. Here we explore divergence of larval morphology in Triturus ivanbureschi, T. macedonicus, and their F1 hybrids. These two genetically and morphologically distinct crested newt species hybridize in nature and form a relatively wide hybrid zone in the central part of the Balkan Peninsula. Using a geometric morphometric approach and multivariate statistics, we evaluated differences of tail size and shape, colouration pattern, and the presence of a tail filament at the mid-larval stage in larvae reared under controlled laboratory conditions. We chose the tail as the main propulsive organ crucial for locomotion, feeding, and escaping predators. We found that Triturus ivanbureschi and T. macedonicus larvae differ in tail shape, but not in tail size. Two groups of F1 hybrid larvae (obtained from reciprocal crossing) were similar to each other, but differed from the parental species in size and shape of the tail, colouration pattern, and the presence of a tail filament. Our results indicate that, like adults, larvae diverge morphologically and hybrid larvae do not exhibit intermediate morphology of the parental species.

Affiliations: 1: 1Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, 11060 Belgrade, Serbia ; 2: 2Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia

*Corresponding author; e-mail: tijana.vucic@ibiss.bg.ac.rs
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1. Ackerly K.L., Ward A.B. (2015): "Linking vertebral number to performance of aquatic escape responses in the axolotl (Ambystoma mexicanum)". Zoology. Vol 118: 394-402. [Crossref]
2. Arntzen J.W. (2003): "Triturus cristatus Superspecies – Kammolch-Artenkreis (Triturus cristatus (Laurenti, 1768) – Nördlicher Kammolch, Triturus carnifex (Laurenti, 1768) – Italienischer Kammolch, Triturus dobrogicus (Kiritzescu, 1903) – Donau-Kammolch, Triturus karelinii (Strauch, 1870) – Südlicher Kammolch)". In: Handbuch der Reptilien und Amphibien Europas. Schwanzlurche IIA, p.  421-514. Böhme W., Ed., Aula-Verlag, Wiebelsheim.
3. Arntzen J.W., Wallis G.P. (1994): "The ‘wolterstorff index’ and its value to the taxonomy of the crested newt superspecies". Abh. Ber. Naturk. Vol 17: 57-66.
4. Arntzen J.W., Wallis G.P. (1999): "Geographic variation and taxonomy of crested newts (Triturus cristatus superspecies): morphological and mitochondrial data". Contribut. Zool. Vol 68: 181-203.
5. Arntzen J.W., Jehle R., Bardakci F., Burke T., Wallis G.P. (2009): "Asymmetric viability of reciprocal-cross hybrids between crested and marbled newts (Triturus cristatus and T. marmoratus)". Evolution. Vol 63: 1191-1202. [Crossref]
6. Arntzen J.W., Wielstra B., Wallis G.P. (2014): "The modality of nine Triturus newt hybrid zones assessed with nuclear, mitochondrial and morphological data". Biol. J. Linn. Soc. Vol 113: 604-622. [Crossref]
7. Arntzen J.W., Beukema W., Galis F., Ivanović A. (2015): "Vertebral number is highly evolvable in salamanders and newts (family Salamandridae) and variably associated with climatic parameters". Contribut. Zool. Vol 84: 85-113.
8. Brede E.G., Thorpe R.S., Arntzen J.W., Langton T.E.S. (2000): "A morphometric study of a hybrid newt population (Triturus cristatus/T. carnifex): Beam Brook Nurseries, Surrey, UK". Biol. J. Linn. Soc. Vol 70: 685-695. [Crossref]
9. Crnobrnja-Isailović J., Džukić G., Krstić N., Kalezić M.L. (1997): "Evolutionary and paleogeographical effects on the distribution of the Triturus cristatus superspecies in the central Balkans". Amphibia-Reptilia. Vol 18: 321-332. [Crossref]
10. Cvijanović M., Ivanović A., Kalezić M.L., Zelditch M.L. (2014): "The ontogenetic origins of skull shape disparity in the Triturus cristatus group". Evol. Dev. Vol 16: 306-317. [Crossref]
11. Cvijanović M., Ivanović A., Kalezić M.L. (2015): "Larval pigmentation patterns of closely related newt species (Triturus cristatus and T. dobrogicus) in laboratory conditions". North-West. J. Zool. Vol 11: 357-359.
12. Dryden I.L., Mardia K.V. (1998): Statistical Analysis of Shape. Wiley.
13. Džukić G., Vukov T.D., Kalezić M.L. (2016): The Tailed Amphibians of Serbia. Belgrade. Serbian Academy of Science and Arts.
14. Escoriza D., Hassine J.B. (2017): "Comparative larval morphology in three species of Pleurodeles (Urodela: Salamandridae)". Zootaxa. Vol 4237: 587-592. [Crossref]
15. Francillon-Vieillot H., Arntzen J.W., Géraudie J. (1990): "Age, growth and longevity of sympatric Triturus cristatus, T. marmoratus and their hybrids (Amphibia, Urodela): a skeletochronological comparison". J. Herpetol. Vol 24: 13-22. [Crossref]
16. Glücksohn S. (1932): "Äußere Entwicklung der Extremitäten und Stadieneinteilung der Larvenperiode von Triton taeniatus Leyd. und von Triton cristatus Laur". Wilhelm Roux’ Archiv f. Entwicklungsmechanik d. Organismen. Vol 125: 341-405. [Crossref]
17. Govedarica P., Cvijanović M., Slijepčević M., Ivanović A. (2017): Trunk elongation and ontogenetic changes in the axial skeleton of Triturus newts. J. Morphol. DOI:10.1002/jmor.20733.
18. Ivanović A., Arntzen J.W. (2014): "Evolution of skull and body shape in Triturus newts reconstructed from three-dimensional morphometric data and phylogeny". Biol. J. Linn. Soc. Vol 113: 243-255. [Crossref]
19. Ivanović A., Vukov T.D., Džukić G., Tomašević N., Kalezić M.L. (2007): "Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae)". Zoomorphology. Vol 126: 173-183. [Crossref]
20. Ivanović A., Sotiropoulos K., Vukov T.D., Eleftherakos K., Džukić G., Polymeni R.M., Kalezić M.L. (2008a): "Cranial shape variation and molecular phylogenetic structure of crested newts (Triturus cristatus superspecies: Caudata, Salamandridae) in the Balkans". Biol. J. Linn. Soc. Vol 95: 348-360. [Crossref]
21. Ivanović A., Tomašević N., Džukić G., Kalezić M.L. (2008b): "Evolutionary diversification of the limb skeleton in crested newts (Triturus cristatus superspecies, Caudata, Salamandridae)". Ann. Zool. Fenn. Vol 45: 527-535. [Crossref]
22. Ivanović A., Cvijanović M., Kalezić M.L. (2011): "Ontogeny of body form and metamorphosis: insights from the crested newts". J. Zool. Vol 283: 153-161. [Crossref]
23. Ivanović A., Üzüm N., Wielstra B., Olgun K., Litvinchuk S.N., Kalezić M.L., Arntzen J.W. (2013): "Is mitochondrial DNA divergence of near eastern crested newts (Triturus karelinii group) reflected by differentiation of skull shape?". Zool. Anz. Vol 252: 269-277. [Crossref]
24. Klingenberg C.P. (2011): "MorphoJ: an integrated software package for geometric morphometrics". Mol. Eco. Resour. Vol 11: 353-357. [Crossref]
25. Laurila A., Karttunen S., Merilä J. (2002): "Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations". Evolution. Vol 56: 617-627. [Crossref]
26. Litvinchuk S.N., Borkin L.J. (2009): Evolution, Systematics and Distribution of Crested Newts (Triturus Cristatus Complex) in the Territory of Russia and Adjacent Countries. Evropeyskiy dom, St. Petersburg.
27. Liu H., Wassersug R., Kawachi K. (1996): "A computational fluid dynamics study of tadpole swimming". J. Exp. Biol. Vol 199: 1245-1260.
28. Monteiro L.R. (1999): "Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape". Syst. Biol. Vol 48: 192-199. [Crossref]
29. Mullin S.K., Taylor P.J. (2002): "The effects of parallax on geometric morphometric data". Comput. Biol. Med. Vol 32: 455-464. [Crossref]
30. Pfennig K.S., Chunco A.J., Lackey A.C. (2007): "Ecological selection and hybrid fitness: hybrids succeed on parental resources". Evol. Ecol. Res. Vol 9: 341-354.
31. Ratnikov V.Y., Litvinchuk S.N. (2007): "Comparative morphology of trunk and sacral vertebrae of tailed amphibians of Russia and adjacent countries". Russ. J. Herpetol. Vol 14: 177-190.
32. Ratnikov V.Y., Litvinchuk S.N. (2009): "Atlantal vertebra of tailed amphibians of Russia and adjacent countries". Russ. J. Herpetol. Vol 16: 57-68.
33. Rohlf F.J. (2006): tpsDig, version 2.26. State Univ. of New York, Stony Brook, New York. Available at: http://life.bio.sunysb.edu/morph/.
34. Rohlf F.J., Slice D. (1990): "Extensions of the Procrustes method for the optimal superimposition of landmarks". Syst. Biol. Vol 39: 40-59.
35. Schmidt B.R., Van Buskirk J. (2005): "A comparative analysis of predator-induced plasticity in larval Triturus newts". J. Evolution. Biol. Vol 18: 415-425. [Crossref]
36. Sheets H.D. (2000): Integrated morphometrics package (IMP). Available at: http://www2.canisius.edu/~sheets.
37. Sherratt E., Vidal-García M., Anstis M., Keogh J.S. (2017): "Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent". Nat. Ecol. Evol. Vol 1: e1385. [Crossref]
38. Slijepčević M., Galis F., Arntzen J.W., Ivanović A. (2015): "Homeotic transformations and number changes in the vertebral column of Triturus newts". PeerJ. Vol 3: e1397. [Crossref]
39. Smith A.B., Littlewood D.T.J., Wray G.A. (1995): "Comparing patterns of evolution: larval and adult life history stages and ribosomal RNA of post-Palaeozoic echinoids". Philos. T. Roy. Soc. B. Vol 349: 11-18. [Crossref]
40. Spurway H. (1953): "Genetics of specific and subspecific differences in European newts". In: Symposia of the Society for Experimental Biology, Number VII. Evolution. Cambridge University Press.
41. Tomašević Kolarov N., Ivanović A., Kalezić M.L. (2011): "Morphological integration and ontogenetic niche shift: a study of crested newt limbs". J. Exp. Zool. Part B. Vol 316: 296-305. [Crossref]
42. Urošević A., Slijepčević M.D., Arntzen J.W., Ivanović A. (2016): "Vertebral shape and body elongation in Triturus newts". Zoology. Vol 119: 439-446. [Crossref]
43. Vallée L. (1959): "Recherches sur Triturus blasii de l’Isle, hybride naturel de Triturus cristatus Laur. x Triturus marmoratus Latr". B. Soc. Zool. Fr. Vol 31: 1-95.
44. Van Buskirk J. (2009): "Natural variation in morphology of larval amphibians: phenotypic plasticity in nature?". Ecol. Monogr. Vol 79: 681-705. [Crossref]
45. Van Buskirk J. (2011): "Amphibian phenotypic variation along a gradient in canopy cover: species differences and plasticity". Oikos. Vol 120: 906-914. [Crossref]
46. Van Buskirk J., McCollum S.A. (2000): "Functional mechanisms of an inducible defense in tadpoles: morphology and behavior influence mortality risk from predation". J. Evolution. Biol. Vol 13: 336-347. [Crossref]
47. Van Buskirk J., Schmidt B.R. (2000): "Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature". Ecology. Vol 81: 3009-3028. [Crossref]
48. Van Buskirk J., McCollum S.A., Werner E.E. (1997): "Natural selection for environmentally induced phenotypes in tadpoles". Evolution. Vol 51: 1983-1992. [Crossref]
49. Van Buskirk J., Anderwald P., Lüpold S., Reinhardt L., Schuler H. (2003): "The lure effect, tadpole tail shape, and the target of dragonfly strikes". J. Herpetol. Vol 37: 420-424. [Crossref]
50. Vinšálková T., Gvoždík L. (2007): "Mismatch between temperature preferences and morphology in F1 hybrid newts (Triturus carnifex × T. dobrogicus)". J. Therm. Biol. Vol 32: 433-439. [Crossref]
51. Vukov T.D., Sotiropoulos K., Wielstra B., Džukić G., Kalezić M.L. (2011): "The evolution of the adult body form of the crested newt (Triturus cristatus superspecies, Caudata, Salamandridae)". J. Zool. Syst. Evol. Res. Vol 49: 324-334. [Crossref]
52. Wassersug R.J. (1989): "Locomotion in amphibian larvae (or “Why aren’t tadpoles built like fishes?”)". Am. Zool. Vol 29: 65-84. [Crossref]
53. Wassersug R.J., Hoff K.V.S. (1985): "The kinematics of swimming in anuran larvae". J. Exp. Biol. Vol 119: 1-30.
54. Webb P.W. (1984): "Body form, locomotion and foraging in aquatic vertebrates". Am. Zool. Vol 24: 107-120. [Crossref]
55. Weihs D. (1989): "Design features and mechanics of axial locomotion in fish". Am. Zool. Vol 29: 151-160. [Crossref]
56. Wielstra B., Arntzen J.W. (2011): "Unraveling the rapid radiation of crested newts (Triturus cristatus superspecies) using complete mitogenomic sequences". BMC Evol. Biol. Vol 11: 162. [Crossref]
57. Wielstra B., Arntzen J.W. (2012): "Postglacial species displacement in Triturus newts deduced from asymmetrically introgressed mitochondrial DNA and ecological niche models". BMC Evol. Biol. Vol 12: 161. [Crossref]
58. Wielstra B., Arntzen J.W. (2014): "Kicking Triturus arntzeni when it’s down: large-scale nuclear genetic data confirm that newts from the type locality are genetically admixed". Zootaxa. Vol 3802: 381-388. [Crossref]
59. Wielstra B., Arntzen J.W. (2016): "Description of a new species of crested newt, previously subsumed in Triturus ivanbureschi (Amphibia: Caudata: Salamandridae)". Zootaxa. Vol 4109: 73-80. [Crossref]
60. Wielstra B., Crnobrnja-Isailović J., Litvinchuk S.N., Reijnen B.T., Skidmore A.K., Sotiropoulos K., Toxopeus A.N., Tzankov N., Vukov T., Arntzen J.W. (2013): "Tracing glacial refugia of Triturus newts based on mitochondrial DNA phylogeography and species distribution modeling". Front. Zool. Vol 10: 13. [Crossref]
61. Wielstra B., Duijm E., Lagler P., Lammers Y., Meilink W.R.M., Ziermann J.M., Arntzen J.W. (2014): "Parallel tagged amplicon sequencing of transcriptome-based genetic markers for Triturus newts with the ion torrent next-generation sequencing platform". Mol. Ecol. Resour. Vol 14: 1080-1089.
62. Wiens J.J., Bonett R.M., Chippindale P.T. (2005): "Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships". Syst. Biol. Vol 54: 91-110. [Crossref]
63. Wolterstorff W. (1923): "Übersicht den Unterarten und Formen des Triton cristatus Laur". Blätter für Aquarien- und Terrarien-kunde. Vol 34: 120-126.
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2018-03-07
2018-09-18

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