TY  - JOUR
AU  - Urošević, Aleksandar
AU  - Ajduković, Maja
AU  - Vučić, Tijana
AU  - Scholtes, Stefan
AU  - Arntzen, Jan, W
AU  - Ivanović, Ana
PY  - 2023
UR  - http://radar.ibiss.bg.ac.rs/handle/123456789/5817
AB  - Serially homologous structures may have complex patterns of regionalization and
morphological integration, influenced by developmental Hox gene expression and
functional constraints. The vertebral column, consisting of a number of repeated,
developmentally constrained, and highly integrated units—vertebrae—is such a
complex serially homologous structure. Functional diversification increases regionalization
and modularity of the vertebral column, particularly in mammals. For
salamanders, three concepts of regionalization of the vertebral column have been
proposed, recognizing one, two, or three presacral regions. Using three‐dimensional
geometric morphometrics on vertebra models acquired with microcomputerized
tomography scanning, we explored the covariation of vertebrae in four closely
related taxa of small‐bodied newts in the genus Lissotriton. The data were analyzed
by segmented linear regression to explore patterns of vertebral regionalization and
by a two‐block partial least squares method to test for morphological integration. All
taxa show a morphological shift posterior to the fifth trunk vertebra, which
corresponds to the two‐region concept. However, morphological integration is
found to be strongest in the mid‐trunk. Taken jointly, these results indicate a highly
integrated presacral vertebral column with a subtle two‐region differentiation. The
results are discussed in relation to specific functional requirements, developmental
and phylogenetic constraints, and specific requirements posed by a biphasic life
cycle and different locomotor modes (swimming vs. walking). Further research
should be conducted on different ontogenetic stages and closely related but
ecologically differentiated species.
PB  - John Wiley and Sons Inc
T2  - Journal of Experimental Zoology Part B - Molecular and Developmental Evolution
T1  - Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton)
VL  - 2023
DO  - 10.1002/jez.b.23205
ER  - 

@article{
author = "Urošević, Aleksandar and Ajduković, Maja and Vučić, Tijana and Scholtes, Stefan and Arntzen, Jan, W and Ivanović, Ana",
year = "2023",
abstract = "Serially homologous structures may have complex patterns of regionalization and
morphological integration, influenced by developmental Hox gene expression and
functional constraints. The vertebral column, consisting of a number of repeated,
developmentally constrained, and highly integrated units—vertebrae—is such a
complex serially homologous structure. Functional diversification increases regionalization
and modularity of the vertebral column, particularly in mammals. For
salamanders, three concepts of regionalization of the vertebral column have been
proposed, recognizing one, two, or three presacral regions. Using three‐dimensional
geometric morphometrics on vertebra models acquired with microcomputerized
tomography scanning, we explored the covariation of vertebrae in four closely
related taxa of small‐bodied newts in the genus Lissotriton. The data were analyzed
by segmented linear regression to explore patterns of vertebral regionalization and
by a two‐block partial least squares method to test for morphological integration. All
taxa show a morphological shift posterior to the fifth trunk vertebra, which
corresponds to the two‐region concept. However, morphological integration is
found to be strongest in the mid‐trunk. Taken jointly, these results indicate a highly
integrated presacral vertebral column with a subtle two‐region differentiation. The
results are discussed in relation to specific functional requirements, developmental
and phylogenetic constraints, and specific requirements posed by a biphasic life
cycle and different locomotor modes (swimming vs. walking). Further research
should be conducted on different ontogenetic stages and closely related but
ecologically differentiated species.",
publisher = "John Wiley and Sons Inc",
journal = "Journal of Experimental Zoology Part B - Molecular and Developmental Evolution",
title = "Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton)",
volume = "2023",
doi = "10.1002/jez.b.23205"
}

Urošević, A., Ajduković, M., Vučić, T., Scholtes, S., Arntzen, J. W.,& Ivanović, A.. (2023). Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton). in Journal of Experimental Zoology Part B - Molecular and Developmental Evolution
John Wiley and Sons Inc., 2023.
https://doi.org/10.1002/jez.b.23205

Urošević A, Ajduković M, Vučić T, Scholtes S, Arntzen JW, Ivanović A. Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton). in Journal of Experimental Zoology Part B - Molecular and Developmental Evolution. 2023;2023.
doi:10.1002/jez.b.23205 .

Urošević, Aleksandar, Ajduković, Maja, Vučić, Tijana, Scholtes, Stefan, Arntzen, Jan, W, Ivanović, Ana, "Regionalization and morphological integration in the vertebral column of Eurasian small‐bodied newts (Salamandridae: Lissotriton)" in Journal of Experimental Zoology Part B - Molecular and Developmental Evolution, 2023 (2023),
https://doi.org/10.1002/jez.b.23205 . .

TY  - CONF
AU  - Urošević, Aleksandar
AU  - Ajduković, Maja
AU  - Vučić, Tijana
AU  - Scholtes, Stefan
AU  - Arntzen, Jan
AU  - Ivanović, Ana
PY  - 2022
UR  - http://radar.ibiss.bg.ac.rs/handle/123456789/5231
AB  - Serially homologous structures, such as the vertebral column, often undergo 
functional and evolutionary diversification and are a good model-system for studies of 
regionalization and morphological integration. We studied these topics in the vertebral 
column (atlas, trunk and sacral vertebrae) of the closely related taxa of small-bodied 
newts – Lissotriton schmidtleri, L. vulgaris ampelensis, L. v. meridionalis and L. v. 
vulgaris, using 3D geometric morphometrics on models that were acquired with micro CT scanning. Two different statistical approaches were employed to test for vertebral 
regionalization and overall morphological integration, namely segmented linear 
regression (SLR) and a partial least squares method (PLS) We observed a common 
pattern of regionalization, with a transition point after the 5th trunk vertebra. It 
corresponds with the antero-posterior transition common for tetrapods. 
Morphological integration, accessed via PLS analysis, is strongest at the 6th and 7th
trunk vertebrae, while the anterior and distal parts of the vertebral column are less 
integrated. The PLS analysis of the asymmetric component of shape variation revealed 
a weak integration, statistically significant only among subsequent trunk vertebrae. In 
summary, the vertebral column of the closely related Lissotriton newts is subtly 
regionalized, while being morphologically integrated overall. There is a complex 
relationship between regionalization and morphological integration of the vertebral 
column, most likely influenced by the newt’s bi-phasic life cycle that instigates different 
functional constraints in the aquatic and terrestrial life stages
PB  - Belgrade: Institute for Biological Research "Siniša Stanković"– National Institute of Republic of Serbia, University of Belgrade
C3  - Program and Book of Abstracts: the 21st European Congress of Herpetology; 2022 Sep 5-9; Belgrade, Serbia
T1  - Vertebral regionalization vs. morphological integration in Lissotriton newts
SP  - 38
UR  - https://hdl.handle.net/21.15107/rcub_ibiss_5231
ER  - 

@conference{
author = "Urošević, Aleksandar and Ajduković, Maja and Vučić, Tijana and Scholtes, Stefan and Arntzen, Jan and Ivanović, Ana",
year = "2022",
abstract = "Serially homologous structures, such as the vertebral column, often undergo 
functional and evolutionary diversification and are a good model-system for studies of 
regionalization and morphological integration. We studied these topics in the vertebral 
column (atlas, trunk and sacral vertebrae) of the closely related taxa of small-bodied 
newts – Lissotriton schmidtleri, L. vulgaris ampelensis, L. v. meridionalis and L. v. 
vulgaris, using 3D geometric morphometrics on models that were acquired with micro CT scanning. Two different statistical approaches were employed to test for vertebral 
regionalization and overall morphological integration, namely segmented linear 
regression (SLR) and a partial least squares method (PLS) We observed a common 
pattern of regionalization, with a transition point after the 5th trunk vertebra. It 
corresponds with the antero-posterior transition common for tetrapods. 
Morphological integration, accessed via PLS analysis, is strongest at the 6th and 7th
trunk vertebrae, while the anterior and distal parts of the vertebral column are less 
integrated. The PLS analysis of the asymmetric component of shape variation revealed 
a weak integration, statistically significant only among subsequent trunk vertebrae. In 
summary, the vertebral column of the closely related Lissotriton newts is subtly 
regionalized, while being morphologically integrated overall. There is a complex 
relationship between regionalization and morphological integration of the vertebral 
column, most likely influenced by the newt’s bi-phasic life cycle that instigates different 
functional constraints in the aquatic and terrestrial life stages",
publisher = "Belgrade: Institute for Biological Research "Siniša Stanković"– National Institute of Republic of Serbia, University of Belgrade",
journal = "Program and Book of Abstracts: the 21st European Congress of Herpetology; 2022 Sep 5-9; Belgrade, Serbia",
title = "Vertebral regionalization vs. morphological integration in Lissotriton newts",
pages = "38",
url = "https://hdl.handle.net/21.15107/rcub_ibiss_5231"
}

Urošević, A., Ajduković, M., Vučić, T., Scholtes, S., Arntzen, J.,& Ivanović, A.. (2022). Vertebral regionalization vs. morphological integration in Lissotriton newts. in Program and Book of Abstracts: the 21st European Congress of Herpetology; 2022 Sep 5-9; Belgrade, Serbia
Belgrade: Institute for Biological Research "Siniša Stanković"– National Institute of Republic of Serbia, University of Belgrade., 38.
https://hdl.handle.net/21.15107/rcub_ibiss_5231

Urošević A, Ajduković M, Vučić T, Scholtes S, Arntzen J, Ivanović A. Vertebral regionalization vs. morphological integration in Lissotriton newts. in Program and Book of Abstracts: the 21st European Congress of Herpetology; 2022 Sep 5-9; Belgrade, Serbia. 2022;:38.
https://hdl.handle.net/21.15107/rcub_ibiss_5231 .

Urošević, Aleksandar, Ajduković, Maja, Vučić, Tijana, Scholtes, Stefan, Arntzen, Jan, Ivanović, Ana, "Vertebral regionalization vs. morphological integration in Lissotriton newts" in Program and Book of Abstracts: the 21st European Congress of Herpetology; 2022 Sep 5-9; Belgrade, Serbia (2022):38,
https://hdl.handle.net/21.15107/rcub_ibiss_5231 .

TY  - JOUR
AU  - Scholtes, Stefan
AU  - Arntzen, Jan
AU  - Ajduković, Maja
AU  - Ivanović, Ana
PY  - 2021
UR  - https://radar.ibiss.bg.ac.rs/handle/123456789/4660
AB  - The salamander vertebral column is largely undifferentiated, with a series of more or less uniform rib bearing presacral vertebrae traditionally designated as the trunk region. We explored regionalisation of the salamander trunk in seven species and two subspecies of the salamander genus Lissotriton by the combination of micro computed tomography scanning and geometric morphometrics. The detailed information on trunk vertebral shape was subjected to a multidimensional cluster analysis and a phenotypic trajectory analysis. With these complementary approaches, we observed a clear morphological regionalization. Clustering analysis showed that the anterior trunk vertebrae (T1 and T2) have distinct morphologies that are shared by all taxa, whereas the subsequent, more posterior vertebrae show significant disparity between species. The phenotypic trajectory analysis revealed that all taxa share a common pattern and amount of shape change along the trunk region. Altogether, our results support the hypothesis of a conserved anterior-posterior developmental patterning which can be associated with different functional demands, reflecting (sub)species’ and possibly, regional ecological divergences within species.
PB  - Hoboken: Wiley
T2  - Journal of Anatomy
T1  - Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region
DO  - 10.1111/joa.13591
ER  - 

@article{
author = "Scholtes, Stefan and Arntzen, Jan and Ajduković, Maja and Ivanović, Ana",
year = "2021",
abstract = "The salamander vertebral column is largely undifferentiated, with a series of more or less uniform rib bearing presacral vertebrae traditionally designated as the trunk region. We explored regionalisation of the salamander trunk in seven species and two subspecies of the salamander genus Lissotriton by the combination of micro computed tomography scanning and geometric morphometrics. The detailed information on trunk vertebral shape was subjected to a multidimensional cluster analysis and a phenotypic trajectory analysis. With these complementary approaches, we observed a clear morphological regionalization. Clustering analysis showed that the anterior trunk vertebrae (T1 and T2) have distinct morphologies that are shared by all taxa, whereas the subsequent, more posterior vertebrae show significant disparity between species. The phenotypic trajectory analysis revealed that all taxa share a common pattern and amount of shape change along the trunk region. Altogether, our results support the hypothesis of a conserved anterior-posterior developmental patterning which can be associated with different functional demands, reflecting (sub)species’ and possibly, regional ecological divergences within species.",
publisher = "Hoboken: Wiley",
journal = "Journal of Anatomy",
title = "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region",
doi = "10.1111/joa.13591"
}

Scholtes, S., Arntzen, J., Ajduković, M.,& Ivanović, A.. (2021). Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region. in Journal of Anatomy
Hoboken: Wiley..
https://doi.org/10.1111/joa.13591

Scholtes S, Arntzen J, Ajduković M, Ivanović A. Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region. in Journal of Anatomy. 2021;.
doi:10.1111/joa.13591 .

Scholtes, Stefan, Arntzen, Jan, Ajduković, Maja, Ivanović, Ana, "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region" in Journal of Anatomy (2021),
https://doi.org/10.1111/joa.13591 . .

TY  - DATA
AU  - Scholtes, Stefan
AU  - Willem, Jan
AU  - Ivanović, Ana
AU  - Ajduković, Maja
PY  - 2021
UR  - https://radar.ibiss.bg.ac.rs/handle/123456789/4661
AB  - Raw landmark coordinates
Each trunk vertebrae (T1 to T13) per species obtained from landmarking 3D surface models of the specimens used in this study can be found in the zip file "Raw landmark coordinates.rar". Each file is labelled as follows: Vertebrae-"Species"-"Collection label"-"Vertebrae number". For example "Vertebrae-Ampelensis-OZ-62-G22595-T1". Collection labels can be found in Appendix table S1 and individual landmark descriptions in Appendix table S2.

Appendix table S1
Collection material analyzed and type of preservation: ethanol preserved and whole-mounts glycerine stored skeletons. Museum codes are: IBISS – University of Belgrade, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia, RMNH.RENA and ZMA.RENA – Naturalis Biodiversity Center, Leiden, The Netherlands. N - sample size.

Appendix table S2
Brief anatomical descriptions of 27 landmarks configured to Lissotriton trunk vertebrae.

Appendix table S3
Frequency (%) of morphotypes over Lissotriton taxon / population and vertebra number.

Appendix table S4
Results on the phenotypic trajectory analysis with P-values for pairwise statistical assessment of a) the amount of species-specific shape changes along trunk region, i.e., trajectory size, b) the general orientation of shape changes in multivariate shape space, i.e., trajectory direction and c) the pattern of shape changes of vertebrae along the trunk region, i.e., trajectory shape.

Supplementary figure S1

Geographical distribution of the (sub-)species of the genus Lissotriton after Arntzen et al., 2009, Ianella et al., 2017 and Wielstra et al.,2018. Taxa are coded by colours as shown in the legend. Numbered dots indicate the localities of the populations that were studied, as also listed in Supplementary table S1. Note that no material was available for L. italicus and L. lantzi.


Supplementary figure S2

Phenotypic trajectories of shape changes along the trunk region of the newt genus Lissotriton expressed over the first (PC1) and third principal component axis (PC3). Trajectories were calculated for nine (sub-)species. The three populations of the L. helveticus were analysed separately. Taxa are coded by colours as shown in the legend. Connected dots represent the mean vertebrae (T) shape from T1 to T12, as is highlighted for L. helveticus from Marcillé la Ville, France. Three-dimensional surface models visualize the corresponding shape changes.


Supplementary figure S2_3D.

Three-dimensional graph showing phenotypic trajectories of shape changes along the trunk region in nine (sub-)species of the newt genus Lissotriton. Open the file with a web browser such as Google Chrome or Mozilla Firefox to visualize the trajectories in three dimensional morphospace that as defined by the first, second and third principal component axis (PC1, PC2 and PC3).
PB  - Hoboken: Wiley
T2  - Journal of Anatomy
T1  - Supplementary material "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region"
DO  - 10.6084/m9.figshare.14254406
ER  - 

@misc{
author = "Scholtes, Stefan and Willem, Jan and Ivanović, Ana and Ajduković, Maja",
year = "2021",
abstract = "Raw landmark coordinates
Each trunk vertebrae (T1 to T13) per species obtained from landmarking 3D surface models of the specimens used in this study can be found in the zip file "Raw landmark coordinates.rar". Each file is labelled as follows: Vertebrae-"Species"-"Collection label"-"Vertebrae number". For example "Vertebrae-Ampelensis-OZ-62-G22595-T1". Collection labels can be found in Appendix table S1 and individual landmark descriptions in Appendix table S2.

Appendix table S1
Collection material analyzed and type of preservation: ethanol preserved and whole-mounts glycerine stored skeletons. Museum codes are: IBISS – University of Belgrade, Institute for Biological Research “Siniša Stanković” – National Institute of Republic of Serbia, RMNH.RENA and ZMA.RENA – Naturalis Biodiversity Center, Leiden, The Netherlands. N - sample size.

Appendix table S2
Brief anatomical descriptions of 27 landmarks configured to Lissotriton trunk vertebrae.

Appendix table S3
Frequency (%) of morphotypes over Lissotriton taxon / population and vertebra number.

Appendix table S4
Results on the phenotypic trajectory analysis with P-values for pairwise statistical assessment of a) the amount of species-specific shape changes along trunk region, i.e., trajectory size, b) the general orientation of shape changes in multivariate shape space, i.e., trajectory direction and c) the pattern of shape changes of vertebrae along the trunk region, i.e., trajectory shape.

Supplementary figure S1

Geographical distribution of the (sub-)species of the genus Lissotriton after Arntzen et al., 2009, Ianella et al., 2017 and Wielstra et al.,2018. Taxa are coded by colours as shown in the legend. Numbered dots indicate the localities of the populations that were studied, as also listed in Supplementary table S1. Note that no material was available for L. italicus and L. lantzi.


Supplementary figure S2

Phenotypic trajectories of shape changes along the trunk region of the newt genus Lissotriton expressed over the first (PC1) and third principal component axis (PC3). Trajectories were calculated for nine (sub-)species. The three populations of the L. helveticus were analysed separately. Taxa are coded by colours as shown in the legend. Connected dots represent the mean vertebrae (T) shape from T1 to T12, as is highlighted for L. helveticus from Marcillé la Ville, France. Three-dimensional surface models visualize the corresponding shape changes.


Supplementary figure S2_3D.

Three-dimensional graph showing phenotypic trajectories of shape changes along the trunk region in nine (sub-)species of the newt genus Lissotriton. Open the file with a web browser such as Google Chrome or Mozilla Firefox to visualize the trajectories in three dimensional morphospace that as defined by the first, second and third principal component axis (PC1, PC2 and PC3).",
publisher = "Hoboken: Wiley",
journal = "Journal of Anatomy",
title = "Supplementary material "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region"",
doi = "10.6084/m9.figshare.14254406"
}

Scholtes, S., Willem, J., Ivanović, A.,& Ajduković, M.. (2021). Supplementary material "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region". in Journal of Anatomy
Hoboken: Wiley..
https://doi.org/10.6084/m9.figshare.14254406

Scholtes S, Willem J, Ivanović A, Ajduković M. Supplementary material "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region". in Journal of Anatomy. 2021;.
doi:10.6084/m9.figshare.14254406 .

Scholtes, Stefan, Willem, Jan, Ivanović, Ana, Ajduković, Maja, "Supplementary material "Variation in vertebrae shape across small-bodied newts reveals functional and developmental constraints acting upon the trunk region"" in Journal of Anatomy (2021),
https://doi.org/10.6084/m9.figshare.14254406 . .