Carapace shape variation of genetically divergent populations of Testudo hermanni boettgeri (Reptilia: Testudines)

Authors

Keywords:

cytb mtDNA, geometric morphometrics, landscape genetics, subspecies, turtle

Abstract

Paper description:

  • Molecular markers, qualitative traits and linear morphometrics disagree on the taxonomical recognition of Balkan’s Hermann’s tortoise (“Testudo hercegovinensis”) populations along the eastern Adriatic Sea coast.
  • For the first time, we analyzed the available genetic data and de novo sequences of cytb mtDNA from Trebinje (type locality of “Testudo hercegovinensis”, Bosnia and Herzegovina) and the Pčinja River Valley (an area of great conservation importance in Serbia), using a landscape genetic approach. We provide data on morphological (carapace) variability of two populations obtained by geometric morphometrics.
  • The implemented approaches argue for genetic and morphological distinctiveness of two allopatric populations.
  • Based on cytb mtDNA, the populations from Pčinja and Trebinje belong to divergent genetical clusters within nominal eastern subspecies Testudo hermanni boettgeri.

Abstract: The published cytb mtDNA sequences from a previous phylogeographic study of Testudo hermanni and de novo genetic and phenotypic data of samples from the Pčinja River Valley (Serbia, Central Balkans) and Trebinje (Bosnia and Herzegovina) were used to: (i) genetically characterize samples from Pčinja, a region of great importance from the conservation standpoint due to its taxonomic diversity and biogeographical history, and Trebinje, a type locality of a disputed taxon “Testudo hercegoviensis” Werner, 1899; (ii) to study the link between gene genealogy and geographic distribution by implementing spatial genetic analyses, and (iii) to assess whether the distribution of carapace shape variation is in accordance with genetic clusters. The samples from Pčinja and Trebinje possessed divergent haplotypes that corresponded to east (HI) and west (HV) genetic clusters, respectively. Geometric morphometrics was found to be a suitable method to distinguish divergent genetic clusters, arguing for the reassessment of a subspecific ranking within the currently recognized eastern Hermann’s subspecies, T. h. boettgeri.

https://doi.org/10.2298/ABS190604043D

Received: June 4, 2019; Revised: July 5, 2019; Accepted: July 15, 2019; Published online: July 25, 2019

How to cite this article: Đurakić MR, Milankov VR. Carapace shape variation of genetically divergent populations of Testudo hermanni boettgeri (Reptilia: Testudines). Arch Biol Sci. 2019;71(4):609-19.

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References

Huang W, Feng S, Liu C, Chen J, Chen J, Chen F. Changes of climate regimes during the last millennium and the twenty-first century simulated by the community earth system model. Quat Sci Rev. 2018;180:42-56.

Todd B, Willson J, Gibbons J. The Global status of reptiles and causes of their decline. In: Sparling DW, Linder G, Bishop CA, Krest S, editors. Ecotoxicology of amphibians and reptiles. 2nd ed. Pensacola, FL, USA: CRC Press; 2010. p. 47-67.

Rhodin AGJ, Stanford CB, van Dijk PP, Eisemberg C, Luiselli L, Mittermeier RA, Hudson R, Horne BD, Goode EV, Kuchling G, Walde A, Baard EHW, Berry KH, Bertolero A, Blanck TEG, Bour R, Buhlmann KA, Cayot LJ, Collett S, Currylow A, Das I, Diagne T, Ennen JR, Forero-Medina G, Frankel MG, Fritz U, García G, Gibbons JW, Gibbons PM, Shiping G, Guntoro J, Hofmeyr MD, Iverson JB, Kiester AR, Lau M, Lawson DP, Lovich JE, Moll EO, Páez VP, Palomo-Ramos R, Platt K, Platt SG, Pritchard PCH, Quinn HR, Rahman SC, Randrianjafizanaka ST, Schaffer J, Selman W, Shaffer HB, Sharma DSK, Haitao S, Singh S, Spencer R, Stannard K, Sutcliffe S, Thomson S, Vogt RC.. Global conservation status of turtles and tortoises (Order Testudines). Chelonian Conserv Biol. 2018;17(2):135.

Bertolero AM, Cheylan A, Hailey A, Livoreil, Willemsen RE. Testudo hermanni ( Gmelin 1789) Hermann’s Tortoise. In: Rhodin A, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA., editors. Biol Freshw Turt Tortoises Compil Proj Int Union Conserv Nat Species Surviv Comm Tortoise Freshw Spec Group. Chelonian Research Monographs. Lunenburg, Massachusetts, USA: Chelonian Research Foundation; 2011. p. 59.1-59.20.

Arnold N, Ovenden D. Reptiles and amphibians of Britain and Europe. London: Collins; 2002. 272 p.

Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403(6772):853-8.

van Dijk PP, Corti C, Mellado VP, Cheylan M. Testudo hermanni. The IUCN Red List of Threatened Species [Internet]. IUCN Red List Threat. Species. 2004 [cited 2019 July]. Available: http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T21648A9306057.

Nikolić S, Golubović A, Bonnet X, Arsovski D, Ballouard J-M, Ajtić R, Sterijovski B, Iković V, Vujović A, Tomović Lj. Why an apparent prosperous subspecies needs strict protection? The case of Testudo hermanni boettgeri from the central Balkans. Herpetol Conserv Biol. 2018;13(3):673-90.

Zenboudji S, Cheylan M, Arnal V, Bertolero A, Leblois R, Astruc G, Bertorelle G, Pretus JL, Lo Valvo M, Sotgiu G, Montgelard C. Conservation of the endangered Mediterranean tortoise Testudo hermanni hermanni: The contribution of population genetics and historical demography. Biol Conserv. 2016;195:279-91.

Ljubisavljević K, Džukić G, Kalezić ML. The commercial export of the land tortoises (Testudo spp.) from the territory of the former Yugoslavia: A historical review and the impact of overharvesting on wild populations. North West J Zool. 2011;7(2):250-60.

Iosif R, Iosif R, Rozylowicz L, Iosif R, Rozylowicz L, Popescu VD. Modeling road mortality hotspots of Eastern Hermann’s tortoise in Romania. Amphibia-Reptilia. 2013;34(2):163-72.

Fritz U, Havaš P. Checklist of Chelonians of the World. Vertebr Zool. 2007;57(2):148-368.

Wermuth H. Testudo hermanni robertmertensi n.subsp. und ihr Vorkommen in Spanien. Senckenbergiana. 1952;33(1/3):157-64.

Perälä J. Biodiversity in relatively neglected taxa of Testudo L., 1758 s.l. Chelonii. 2001;3:40-53.

Perälä J. Testudo hercegovinensis Werner, 1899. Manouria. 2004;7:19-20.

Werner F. Beiträge zur Kenntnis der reptilien- und Batrachierfauna der Balkanhalbinsel. Wiss Mitt Bosn Herzeg. 1899;6:817-41.

Bour R. Testudo boettgeri Mojsisovics, 1889. Manouria. 2004;7(22):9-10.

Bour R. A new character for the identification of populations of the Hermann’s tortoise, Testudo hermanni Gmelin, 1789. Salamandra. 2004;40:59-66.

Vetter H. Hermann’s Tortoise, Boettger’s and Dalmatian Tortoises. Frankfurt am Main: Edition Chimaira; 2006. 325 p.

Fritz U, Auer M, Bertolero A, Cheylan M, Fattizzo T, Hundsdorfer AK, Martin Sampayo M, Pretus JL, Široký P, Wink M. A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zool Scr. 2006;35(5):531-43.

Pettengill JB, Moeller DA. Phylogeography of speciation: Allopatric divergence and secondary contact between outcrossing and selfing Clarkia. Mol Ecol. 2012;21(18):4578-92.

Patten MA. Subspecies and the philosophy of science. Auk. 2015;132(2):481-5.

Vinarski M V. The fate of subspecies category in Zoological systematics. 1. The history. Biol Bull Rev. 2015;5(5):395-404.

Vinarski M V. The fate of subspecies category in Zoological systematics. 2. The present. Biol Bull Rev. 2015;5(5):405-14.

Karanovic T, Djurakic M, Eberhard SM. Cryptic species or inadequate taxonomy? Implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa. Syst Biol. 2016;65(2):304-27.

Petrović J, Dragović S, Dragović R, Đorđević M, Đokić M, Zlatković B, Walling D. Using 137Cs measurements to estimate soil erosion rates in the Pčinja and South Morava River Basins, southeastern Serbia. J Environ Radioact. 2016;158-159:71-80.

Tomović Lj, Ajtić R, Ljubisavljević K, Urošević A, Jović D, Krizmanić I, Labus N, Đorđević S, Kalezić ML, Vukov T, Džukić G. Reptiles in Serbia - distribution and diversity patterns. Bull Nat Hist Museum. 2014;7:129-58.

Tomović Lj, Urošević A, Ajtić R, Krizmanić I, Simovic A, Labus N, Jović D, Krstić M, Đorđević S, Anđelković M, Golubović A, Džukić G. Contribution to the knowledge of distribution of Colubrid snakes in Serbia. Ecol Montenegrina. 2015;2(3):162-86.

Zlatković B, Nikolić L, Ranđelović V, Ranđelović N, Stevanović V. Comparative analyses of the vascular flora of the Pčinja river gorges in Serbia and Macedonia. Arch Biol Sci. 2011;63(4):1157-66.

Guillot G, Renaud S, Ledevin R, Michaux J, Claude J. A unifying model for the analysis of phenotypic, genetic, and geographic data. Syst Biol. 2012;61(5):897-911.

Guillot G, Mortier F, Estoup A. GENELAND: A computer package for landscape genetics. Mol Ecol Notes. 2005;5(3):712-5.

Stubbs D, Swingland IR, Hailey A, Pulford E. The ecology of the mediterranean tortoise Testudo hermanni in northern Greece (the effects of a catastrophe on population structure and density). Biol Conserv. 1985;31(2):125-52.

Juste JB, Álvarez Y, Tabarés E, Garrido-Pertierra A, Ibáñez C, Bautista JM. Phylogeography of African Fruitbats (Megachiroptera). Mol Phylogenet Evol . 1999;13(3):596-604.

Fritz U, Alcalde L, Vargas-Ramírez M, Goode EV, Fabius-Turoblin DU, Praschag P. Northern genetic richness and southern purity, but just one species in the Chelonoidis chilensis complex. Zool Scr. 2012;41(3):220-32.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547-9.

Templeton AR, Crandall KA, Sing CF. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics. 1992;132:619-633.

Paradis E. Analysis of haplotype networks: The randomized minimum spanning tree method. Methods Ecol Evol. 2018;9(5):1308-17.

Paradis E. Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26(3):419-20.

Guillot G. Inference of structure in subdivided populations at low levels of genetic differentiation - The correlated allele frequencies model revisited. Bioinformatics. 2008;24(19):2222-8.

Guillot G, Santos F, Estoup A. Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics. 2008;24(11):1406-7.

Rohlf FJ. The tps series of software. Hystrix. 2015;26(1):1-4.

Adams DC, Rohlf FJ, Slice DE. A field comes of age: Geometric morphometrics in the 21st century. Hystrix. 2013;24(1):7-14.

Rohlf JF, Slice D. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool. 1990;39(1):40

Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution. 2002; 56(10):1909-20.

Cardini A. Lost in the other half: improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Syst Biol. 2016;65(6):1096-106.

Adams DC, Otárola-Castillo E. geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 2013;4: 393–9.

Collyer ML, Adams DC. RRPP : An r package for fitting linear models to high-dimensional data using residual randomization. Methods Ecol Evol. 2018;9(7):1772-9.

Collyer ML, Sekora DJ, Adams DC. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity. 2015;115:357-65.

Klingenberg CP. Visualizations in geometric morphometrics: How to read and how to make graphs showing shape changes. Hystrix. 2013;24(1):15-24.

Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11(2):353-7.

Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool. 2007;4(1):11.

Grabowski M, Mamos T, Bącela-Spychalska K, Rewicz T, Wattier RA. Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod. PeerJ. 2017;5:e3016.

Kuratani S, Nagashima H. A developmental basis for innovative evolution of the turtle shell. In: Asher RJ, Müller J, editors. From clone to bone: the synergy of morphological and molecular tools in palaeobiology. Cambridge: University Press; 2012.

McIntyre DC, Rakshit S, Yallowitz AR, Loken L, Jeannotte L, Capecchi MR, Wellik DM. Hox patterning of the vertebrate rib cage. Development. 2007;134(16):2981-9.

Djordjević S, Tomović Lj, Golubović A, Simovic A, Sterijovski B, Djurakic M, Bonnet X. Geographic (in-)variability of gender-specific traits in Hermann’s tortoise. Herpetol J. 2013;23(2):67.

Rissler LJ. Union of phylogeography and landscape genetics. Proc Natl Acad Sci. 2016;113(29):8079-86.

Kindler C, Fritz U. Phylogeography and taxonomy of the barred grass snake (Natrix helvetica), with a discussion of the subspecies category in zoology. Vertebr Zool. 2018;68(3):269-81.

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Published

2019-12-19

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Đurakić MR, Milankov VR. Carapace shape variation of genetically divergent populations of Testudo hermanni boettgeri (Reptilia: Testudines). Arch Biol Sci [Internet]. 2019Dec.19 [cited 2022Aug.18];71(4):609-1. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/4345

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