# Species Distribution Models and Niche Partitioning among Unisexual Darevskia dahli and Its Parental Bisexual (D. portschinskii, D. mixta) Rock Lizards in the Caucasus

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## Abstract

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## 1. Introduction

## 2. Materials and Methods

#### 2.1. Dataset Acquisition and Preparation of Vector and Raster Layers

#### 2.2. Spatial Thinning of Records and Predictor Variables

#### 2.3. Determination of the Maxent Models Parameters

#### 2.4. Construction of Species Distribution (SDM) and Ecological Niche (ENM) Models

_{ind}) to assess model performance [69,70,71] with the help of the EcoSpat R package [71]. Boyce index lacks those drawbacks which has AUC index [72,73]. It requires only data on lizard occurrence and measures how much the predictive models differ from random distribution. We calculated B

_{ind}for all the 10 models for each lizard; afterwards we averaged the obtained values to get the final estimates. The importance of each predictor variable of SDMs was assessed by analysis of Maxents variable contribution table using the jackknife method [45,46]. Variables with essential impact on the model, i.e., having high values of permutation importance (PI > 5) and/or high values of the percent of contribution (PC > 5) were considered as the most important.

#### 2.5. Comparison of Ecological Niches and Parameters of Habitat Exploitation

_{b}). The difference in the niches breadth was estimated in two steps. First, the uniformity of the niches breadth was tested using multiple comparisons [77]. Then, if the null hypothesis was rejected, niches were compared pairwise [78].

## 3. Results

#### 3.1. Model Performance and Predictor Variables

_{ind}were obtained based on Maxent parameters by default and using the optimal parameters determined by AICc test (Delta AIC < 2) (Supplementary Figure S3). As a result, B

_{ind}significantly differed between these two versions of SDMs. Boyce Index (B

_{ind}± SE) for SDMs of D. dahli, D. portschinskii and D. mixta calculated with Maxent parameters by default were 0.938 (±0.0012), 0.91 (±0.003), 0.91 (0.004), respectively, and for optimal parameters of Maxent, they were 0.95 (±0.004), 0.93 (±0.004) and 0.94 (±0.003), respectively. A statistically significant increase in SDMs performance (B

_{ind}) was found for all studied species: D. dahli (t = 2.82, p = 0.006), D. portschinskii (t = 4.83, p << 0.001) and D. mixta (t = 7.13, p << 0.001). To conclude, the settings by default resulted in more complex and less accurate SDMs.

_{ind}at optimal parameters of Maxent are given in Table 2. These results show that three variables, namely precipitation of the warm quarter (C_PWarmQ), solar irradiation (C_SRad) and elevation (T_EL), are significant for all species. The remaining predictor variables determining the suitable habitats varied among the species. The habitat preferences of D. dahli determined by isothermality (C_ISOT) and distance to road (L_DHW); while the “paternal” species D. portschinskii depends on isothermality (C_ISOT), seasonal coefficient of humidity variation (C_PCoefVar), annual temperature range (C_TAnR), air temperature in dry quarter (C_MTDrQ), distance to road (L_DHW), and vegetation type (L_VEG). The habitat preferences of D. mixta, mainly depend on the seasonal coefficient of humidity variation (C_PCoefVar) and vegetation type (L_VEG). There are three common predictor variables for D. dahli and D. mixta (Table 2). All the variables responsible for D. dahli preferences are relevant for D. portschinskii except for vegetation type.

#### 3.2. Potential Range of Studied Lizards

#### 3.3. Comparative Analysis of Ecological Niches

_{b}= 1.12 (±0.15), the intermediate breadth was in D. dahli, Nb = 0.86 (±0.12), and the smallest breadth was in D. mixta, Nb = 0.48 (±0.08). The pairwise comparison showed that N

_{b}in D. portschinskii was significantly wider (F = 1.31, p = 0.026) while that of the D. mixta was narrower (F = 2.27, p = 0.0001) than in D. dahli. The largest standard deviations of MD (SD MD = 10.1) was for D. portschinskii, the intermediate (SD MD = 9.4) for D. dahli, and smallest (SD MD = 5.1) was obtained for D. mixta. The largest distance between the niche centroids MD = 21.1 was found between the parental species (D. portschinskii and D. mixta), the intermediate MD = 16.5 was observed between the centroids of D. mixta and D. dahli, and the smallest MD = 0.78 was obtained between the centroids of D. portschinskii and D. dahli.

#### 3.4. Shifts of Ecological Niches Centroids along Environmental Gradients

#### 3.5. Statistical Analysis of the Shifts of Niche Centroids

^{−2}day

^{−1}), and large distance from roads (774 ± 34 m).

^{−2}day

^{−1}) (Figure 3h), medium coefficient of humidity variation (44 ± 0.48%) (Figure 3f), low total annual precipitation (630 ± 9mm) (Figure 3e), and low total precipitation in the warm season (192 ± 3 mm) (Figure 3e). In terms of distance roads, D. portschinskii occupies an intermediate position relative to the other lizards (540 ± 17 m) (Figure 3j).

^{−2}day

^{−1}) (Figure 3h), high seasonal variation of humidity (46 ± 0.6%) (Figure 3f), and low average temperatures in dry quarter of year (0.09 ± 0.33 °C) (Figure 3d). Habitats of D. dahli are located close to roads (514 ± 22 m) (Figure 3j).

## 4. Discussion

#### 4.1. Predicted Distribution Range with Optimal Model Parameters

#### 4.2. Niches of the Unisexual and Bisexual Lizards: Breadth, Overlap, Similarity and Shifts

#### 4.3. Mechanisms of Coexistence of Unisexual and Bisexual Forms

## 5. Conclusions

_{ind}) for all studied lizards calculated with optimal Maxent parameters using AICc criterion evidenced that we were able to select the most important environmental predictor variables that determine habitat suitability for lizards. The narrow niche breadth of the “maternal” species D. mixta relative to that of D. dahli, and separation of their habitats confirm that the initial assumption of GP model was fulfilled. However, the fact of the displacement of D. mixta from its native range by polyphyletic clones of D. dahli has not been completely proven and requires further studies. On the other hand, the availability of polyphyletic clones, a significant superiority in the niche breadth of the “paternal” species D. portschinskii, and significant shifts of the niche centroids of clonal forms facilitate co-existence of these species in the Caucasus. We regard the differentiation of unisexual and bisexual lizards’ niches as a mechanism of their survival. Finally, we developed a new methodological approach based on the SDMs and ENMs which can be further applied for studying the niche partitioning in unisexual and its parental bisexual forms. These results can be helpful for conducting future field surveys and can be used by environmental agencies and/or decision makers to preserve natural habitats for rock lizards.

## Supplementary Materials

**a**), (

**c**), (

**e**) are initial clustered data sets; (

**b**), (

**d**), (

**f**) are reduced non–autocorrelated data sets. Dotted areas represent masks used to fit the potential distribution models of Darevskia spp. Figure S2: Evaluation metrics for D. dahli, D. portschinskii и D. mixta resulting from MaxEnt models made across a range of feature-class combinations and regularization multipliers. AICc is the Akaike Information Criterion corrected for small sample sizes, delta AICc (DAIC) is the difference between the AICc of a given model and the AICc of the model with the lowest AICc. Dotted horizontal line represents delta AICc = 2, which delimits models that are generally considered to have substantial support relative to others examined – that is those below the line. Default settings and settings that yielded minimum AICc are indicated with arrows. Legends denote feature classes allowed (L = linear, Q = quadratic, H = hinge, p = product and T = threshold). Note that for these lizards, AICc consistently selected regularization multipliers higher than the default value. Figure S3: Relationships between each of the most important environmental predictors (see Table 2) and the likelihood of D. dahli occurrence. Figure S4: Relationships between each of the most important environmental predictors (see Table 2) and the likelihood of D. portschinskii occurrence. Vegetation type: 1—Mountain forest zone, 2—Mountain meadows, 3—Mountain steppe, 4—Arid mountain steppe, 5—Nival zone, 6—Semi-desert, 7—Cultivated areas, 8—Wetland areas, 9—Alpine zone, 10—Urban areas. Figure S5: Relationships between each of the most important environmental predictors (see Table 2) and the likelihood of D. mixta occurrence. Vegetation types are presented in Figure S4. Figure S6: Correlation between predictor variables and the first two components of the principal component analysis calibrated on the environmental conditions in parental and “daughter” lizards. First and second components explain 81.1% of the total variation. The abbreviations of variables are described in Table S1. Figure S7: Graphic representation of the shift of the niche centroid of the parthenogenetic lizard D. dahli relative to the “maternal” species D. mixta along the most important environmental gradients. The red arrow indicates the direction of niches shift. Vegetation types are presented in Figure S4. Figure S8: Graphic representation of the shift of the niche centroid of the parthenogenetic lizard D. dahli relative to the “paternal” species D. portschinskii along the most important environmental gradients. The red arrow indicates the direction of niches shift. Vegetation types are presented in Figure S4. Figure S9: Comparing the means positions (centroids) of the ecological niches of the studied rock lizards along the gradients of the environment using Post Hoc Tukey HSD test. Differences between each pair of means are presented with 95% family-wise confidence level. The names of the predictor variables (see Table S1) for the panels (

**a**)–(

**j**) are the same as in Figure 3. Table S1: Habitat variables considered in the species distribution models. Table S2: Average Nearest Neighbor Index (ANNI) of the species occurrence data, where n is the number of sampling sites, Z score is the statistic value showing validity of the null hypothesis of a random distribution of points.

## Author Contributions

## Funding

## Acknowledgments

## Conflicts of Interest

## References

- Fujita, M.; Moritz, C. Origin and evolution of parthenogenetic genomes in lizards: Current state and future directions. Cytogenet. Genome Res.
**2009**, 127, 261–272. [Google Scholar] [CrossRef] [PubMed] - Darevsky, I.S. Rock Lizards of The Caucasus, Systematics, Ecology and Phylogenesis of the Polymorphic Groups of Caucasian Rock Lizards of the Subgenus; Nauka: Leningrad, Russia, 1967. [Google Scholar]
- Borkin, L.J.; Darevsky, I.S. Reticular (hybridogeneous) speciation in vertebrate. Zh. Obshch. Biol.
**1980**, 41, 485–506. [Google Scholar] - Kearney, M.R.; Fujita, M.K.; Ridenour, J. Lost Sex. In the Reptiles: Constraints and Correlations; Springer Science and Business Media LLC: Heidelberg, Germany, 2009; pp. 447–474. [Google Scholar]
- Sinclair, E.A.; Pramuk, J.B.; Bezy, R.L.; Crandall, K.A.; Sites, J.W. DNA evidence for non hybrid origins of parthenogenesis in natural populations of vertebrates. Evolution
**2010**, 64, 1346–1357. [Google Scholar] [PubMed] - West, S. Lively; Read A pluralist approach to sex and recombination. J. Evol. Biol.
**1999**, 12, 1003–1012. [Google Scholar] [CrossRef] [Green Version] - Vrijenhoek, R.C. Unisexual fish: Model systems for studying ecology and evolution. Annu. Rev. Ecol. Syst.
**1994**, 25, 71–96. [Google Scholar] [CrossRef] - Roughgarden, J. Evolution of niche width. Am. Nat.
**1972**, 106, 683–718. [Google Scholar] [CrossRef] - Vrijenhoek, R.C.; Parker, E.D. Geographical Parthenogenesis: General Purpose Genotypes and Frozen Niche Variation. In Lost Sex; Schön, I., Martens, K., Van Dijk, P., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 99–131. [Google Scholar]
- Kearney, M.R. Hybridization, glaciation and geographical parthenogenesis. Trends Ecol. Evol.
**2005**, 20, 495–502. [Google Scholar] [CrossRef] - Peck, J.R.; Yearsley, J.; Waxman, D. Explaining the geographic distributions of sexual and asexual populations. Nature
**1998**, 391, 889–892. [Google Scholar] [CrossRef] - Glesener, R.R.; Tilman, D. Sexuality and the components of environmental uncertainty: Clues from geographic parthenogenesis in terrestrial animals. Am. Nat.
**1978**, 112, 659–673. [Google Scholar] [CrossRef] - Kearney, M.; Wahl, R.; Autumn, K. Increased capacity for sustained locomotion at low temperature in parthenogenetic geckos of hybrid origin. Physiol. Biochem. Zool.
**2005**, 78, 316–324. [Google Scholar] [CrossRef] [Green Version] - Vandel, A. La parthénogenèse géographique contribution a l’ètude biologique et cytologique de la parthénogenèse naturelle. Bull. Biol. Fr. Belg.
**1928**, 62, 164–281. [Google Scholar] - Beaton, M.J. Geographical parthenogenesis and polyploidy in daphnia pulex. Am. Nat.
**1988**, 132, 837–845. [Google Scholar] [CrossRef] - Gray, M.M.; Weeks, S.C. Niche breadth in clonal and sexual fish (Poeciliopsis): A test of the frozen niche variation model. Can. J. Fish. Aquat. Sci.
**2001**, 58, 1313–1318. [Google Scholar] [CrossRef] - Wright, J.W.; Lowe, C.H. Weeds, polyploids, parthenogenesis, and the geographical and ecological distribution of all-female species of cnemidophorus. Copeia
**1968**, 1968, 128–138. [Google Scholar] [CrossRef] - Greenwald, K.R.; Denton, R.D.; Gibbs, H.L. Niche partitioning among sexual and unisexual Ambystoma salamanders. Ecosphere
**2016**, 7, 01579. [Google Scholar] [CrossRef] - Bierzychudek, P. Patterns in plant parthenogenesis. Cell. Mol. Life Sci.
**1985**, 41, 1255–1264. [Google Scholar] [CrossRef] - Hörandl, E. The complex causality of geographical parthenogenesis. New Phytol.
**2006**, 171, 525–538. [Google Scholar] [CrossRef] - Darevsky, I.S. Natural parthenogenesis in polymorphic group of the Caucasian rock lizards related to Lacerta saxicola Eversman. J. Ohio Herpetol. Soc.
**1966**, 5, 115–152. [Google Scholar] [CrossRef] - Murphy, R.W.; Fu, J.; MacCulloch, R.D.; Darevsky, I.S.; Kupriyanova, L.A. A fine line between sex and unisexuality: The phylogenetic constraints on parthenogenesis in lacertid lizards. Zool. J. Linn. Soc-Lond.
**2000**, 130, 527–549. [Google Scholar] [CrossRef] - Vergun, A.A.; Martirosyan, I.A.; Semyenova, S.K.; Omelchenko, A.; Petrosyan, V.G.; Lazebny, O.E.; Tokarskaya, O.N.; Korchagin, V.I.; Ryskov, A. Clonal diversity and clone formation in the parthenogenetic caucasian rock lizard darevskia dahli. PLoS ONE
**2014**, 9, e91674. [Google Scholar] [CrossRef] [Green Version] - Darevsky, I.S. Natural parthenogenesis in certain subspecies of rock lizards (Lacerta saxicola Eversmann). Dokl. Akad. Nauk SSSR Biol. Sci.
**1958**, 122, 730–732. [Google Scholar] - Uzzell, T.; Darevsky, I.S. Biochemical evidence for the hybrid origin of the parthenogenetic species of the lacerta saxicola complex (sauria: Lacertidae), with a discussion of some ecological and evolutionary implications. Copeia
**1975**, 1975, 204–222. [Google Scholar] [CrossRef] - MacCulloch, R.D.; Murphy, R.W.; Fu, J.; Darevsky, I.S.; Danielyan, F. Disjunct habitats as islands: Genetic variability in the Caucasian rock lizard Lacerta portschinskii. Genetica
**1997**, 101, 41–45. [Google Scholar] [CrossRef] [PubMed] - Martirosyan, I.A.; Kan, N.G.; Petrosyan, V.G.; Malysheva, D.N.; Trofimova, A.A.; Danielyan, F.D.; Darevskii, I.S.; Korochkin, L.I.; Ryskov, A.; Tokarskaya, O.N. Variation of mini- and microsatellite DNA repeats in parthenogenetic lizard darevskia armeniaca as revealed by DNA fingerprinting analysis. Russ. J. Genet.
**2003**, 39, 159–165. [Google Scholar] [CrossRef] - Malysheva, D.N.; Vergun, A.A.; Tokarskaya, O.N.; Sevast’Yanova, G.A.; Darevsky, I.S.; Ryskov, A. Nucleotide sequences of the microsatellite locus Du215 (arm) allelic variants in the parthenospecies Darevskia armeniaca (Lacertidae). Russ. J. Genet.
**2007**, 43, 116–120. [Google Scholar] [CrossRef] - Tarkhnishvili, D.; Gavashelishvili, A.; Avaliani, A.; Murtskhvaladze, M.; Mumladze, L. Unisexual rock lizard might be out competing its bisexual progenitors in the Caucasus. Biol. J. Linn. Soc.
**2010**, 101, 447–460. [Google Scholar] [CrossRef] [Green Version] - Arakelyan, M.S.; Danielyan, F.D.; Corti, C.; Sindaco, R.; Leviton, A.E. Herpetofauna of Armenia and Nagorno-Karabakh; Society for Study of Amphibians and Reptiles: Salt Lake City, UT, USA, 2011. [Google Scholar]
- Petrosyan, V.G.; Osipov, F.A.; Bobrov, V.V.; Dergunova, N.N.; Danielyan, F.D.; Arakelyan, M.S. Analysis of geographical distribution of the parthenogenetic rock lizard Darevskia armeniaca and its parental species (D. mixta, D. valentini) based on ecological modelling. Salamandra
**2019**, 55, 173–190. [Google Scholar] - Parker, E.D.; Walker, J.M.; Paulissen, M.A. Clonal Diversity in Cnemidophorus: Ecological and Morphological Consequences. In Evolution and Ecology of Unisexual vertebrates; Dawley, R.M., Bogart, J.P., Eds.; New York State Museum Bulletin: Albany, NY, USA, 1989; Volume 466, pp. 72–86. [Google Scholar]
- Species Complex of the Lacertid Lizards. Available online: https://www.lacerta.de/AS/Taxon.php?Genus=33 (accessed on 9 July 2020).
- Fu, J.; Murphy, R.W.; Darevsky, I.S. Limited genetic variation in Lacerta mixta and its parthenogenetic daughter species: Evidence from cytochrome b and ATPase 6 gene DNA sequences. Genetica
**1999**, 105, 227–231. [Google Scholar] [CrossRef] - Arakelyan, M.; Danielyan, F.; Stepanyan, I. Hybrids of Darevskia valentini, D. armeniaca and D. unisexualis from a sympatric population in Armenia. Amphib.
**2008**, 29, 487–504. [Google Scholar] [CrossRef] [Green Version] - Spangenberg, V.; Arakelyan, M.; Galoyan, E.; Matveevsky, S.; Petrosyan, R.; Bogdanov, Y.; Danielyan, F.; Kolomiets, O. Reticulate evolution of the rock lizards: Meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus darevskia. Genes
**2017**, 8, 149. [Google Scholar] [CrossRef] [Green Version] - Spangenberg, V.; Arakelyan, M.; Galoyan, E.; Pankin, M.; Petrosyan, R.; Stepanyan, I.; Grishaeva, T.; Danielyan, F.; Kolomiets, O. Extraordinary centromeres: Differences in the meiotic chromosomes of two rock lizards species Darevskia portschinskii and Darevskia raddei. Peer J.
**2019**, 7, e6360. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Tarkhnishvili, D.; Murtskhvaladze, M.; Anderson, C.L. Coincidence of genotypes at two loci in two parthenogenetic rock lizards: How backcrosses might trigger adaptive speciation. Biol. J. Linn. Soc.
**2017**, 121, 365–378. [Google Scholar] [CrossRef] - Kaliontzopoulou, A.; Brito, J.C.; Carretero, M.; Larbes, S.; Harris, D.J. Modelling the partially unknown distribution of wall lizards (Podarcis) in North Africa: Ecological affinities, potential areas of occurrence, and methodological constraints. Can. J. Zool.
**2008**, 86, 992–1001. [Google Scholar] [CrossRef] - Pleguezuelos, J.M.; Mora, E.; De Pous, P.; Escoriza, D.; Metallinou, M.; Donaire, D.; Comas, M.; Carranza, S. Elusive but widespread? The potential distribution and genetic variation of Hyalosaurus koellikeri (Günther, 1873) in the Maghreb. Amphib-reptil
**2011**, 32, 385–397. [Google Scholar] [CrossRef] [Green Version] - Ahmadzadeh, F.; Carretero, M.A.; Rödder, D.; Harris, D.J.; Freitas, S.N.; Perera, A.; Böhme, W. Inferring the effects of past climate fluctuations on the distribution pattern of Iranolacerta (Reptilia, Lacertidae): Evidence from mitochondrial DNA and species distribution models. Zool. Anz. A J. Comp. Zool.
**2013**, 252, 141–148. [Google Scholar] [CrossRef] - Doronin, I.V. Distribution data of rock lizards from the Darevskia (praticola) complex (Sauria: Lacertidae). Curr. Stud. Herpetol.
**2015**, 15, 3–38. [Google Scholar] - Freitas, S.N.; Rocha, S.; Campos, J.C.; Ahmadzadeh, F.; Corti, C.; Sillero, N.; Ilgaz, Ç.; Kumlutas, Y.; Arakelyan, M.; Harris, D.J.; et al. Parthenogenesis through the ice ages: A biogeographic analysis of Caucasian rock lizards (genus Darevskia). Mol. Phylogenetics Evol.
**2016**, 102, 117–127. [Google Scholar] [CrossRef] - Ćorović, J.; Popovic, M.; Cogălniceanu, D.; Carretero, M.; Crnobrnja-Isailović, J. Distribution of the meadow lizard in Europe and its realized ecological niche model. J. Nat. Hist.
**2018**, 52, 1909–1925. [Google Scholar] [CrossRef] - Phillips, S.J.; Anderson, R.P.; Schapire, R.E. Maximum entropy modeling of species geographic distributions. Ecol. Model.
**2006**, 190, 231–259. [Google Scholar] [CrossRef] [Green Version] - Phillips, S.J.; Dudík, M. Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography
**2008**, 31, 161–175. [Google Scholar] [CrossRef] - Peterson, A.T.; Soberón, J. Species distribution modeling and ecological niche modeling: Getting the concepts right. Nat. Conserv
**2012**, 10, 102–107. [Google Scholar] [CrossRef] - Melo-Merino, S.M.; Reyes-Bonilla, H.; Lira-Noriega, A. Ecological niche models and species distribution models in marine environments: A literature review and spatial analysis of evidence. Ecol. Model.
**2020**, 415, 108837. [Google Scholar] [CrossRef] - Soberón, J. Grinnellian and Eltonian niches and geographic distributions of species. Ecol. Lett.
**2007**, 10, 1115–1123. [Google Scholar] [CrossRef] [PubMed] - Elith, J.; Graham, C.; Anderson, R.P.; Dudík, M.; Ferrier, S.; Guisan, A.; Hijmans, R.; Huettmann, F.; Leathwick, J.R.; Lehmann, A.; et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography
**2006**, 29, 129–151. [Google Scholar] [CrossRef] [Green Version] - Hernandez, P.A.; Graham, C.; Master, L.L.; Albert, D.L. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography
**2006**, 29, 773–785. [Google Scholar] [CrossRef] - Wisz, M.; Hijmans, R.; Elith, J.; Peterson, A.T.; Graham, C.; Guisan, A. Effects of sample size on the performance of species distribution models. Divers. Distrib.
**2008**, 14, 763–773. [Google Scholar] [CrossRef] - Akaike, H. A new look at the statistical model identification. IEEE Trans. Autom. Control.
**1974**, 19, 716–723. [Google Scholar] [CrossRef] - Muscarella, R.; Galante, P.J.; Soley-Guardia, M.; Boria, R.A.; Kass, J.M.; Uriarte, M.; Anderson, R.P. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol. Evol.
**2014**, 5, 1198–1205. [Google Scholar] [CrossRef] - Global Biodiversity Information Facility. Available online: https://doi.org/10.15468/dl.4wnnka (accessed on 9 July 2020).
- Global Biodiversity Information Facility. Available online: https://doi.org/10.15468/dl.ml4da9 (accessed on 9 July 2020).
- Global Biodiversity Information Facility. Available online: https://doi.org/10.15468/dl.i83b94 (accessed on 9 July 2020).
- Global Climate and Weather Data. Available online: https://www.worldclim.org/data/worldclim21.html (accessed on 9 July 2020).
- Hijmans, R.; Cameron, S.E.; Parra, J.L.; Jones, P.G.; Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Clim.
**2005**, 25, 1965–1978. [Google Scholar] [CrossRef] - Shuttle Radar Topographic Mission. Available online: https://www2.jpl.nasa.gov/srtm (accessed on 9 July 2020).
- Open Street Map. Available online: http://www.openstreetmap.org/ (accessed on 11 December 2011).
- Acopian Center for the Environment GIS Data. Available online: http://ace.aua.am/gis-and-remote-sensing/vector-data (accessed on 9 July 2020).
- Aiello-Lammens, M.E.; Boria, R.A.; Radosavljevic, A.; Vilela, B.; Anderson, R.P.; Silva, D.P. spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography
**2015**, 38, 541–545. [Google Scholar] [CrossRef] - Environmental Systems Research Institute. Arc GIS Desktop 10.6.1. Available online: https://support.esri.com/en/products/desktop/arcgis-desktop/arcmap/10-6-1 (accessed on 9 July 2020).
- Barbosa, A.M. fuzzySim: Applying fuzzy logic to binary similarity indices in ecology. Methods Ecol. Evol.
**2015**, 6, 853–858. [Google Scholar] [CrossRef] - Hair, J.F.; Anderson, R.E., Jr.; Tatham, R.L.; Black, W.C. Multivariate Data Analysis, 3rd ed.; Macmillan: New York, NY, USA, 1995. [Google Scholar]
- Radosavljevic, A.; Anderson, R.P. Making better Maxentmodels of species distributions: Complexity, overfitting and evaluation. J. Biogeogr.
**2013**, 41, 629–643. [Google Scholar] [CrossRef] - Hijmans, R.J.; Phillips, S.; Leathwick, J.; Elith, J. Dismo Package for R. 2017. Available online: https://cran.r-project.org/package=dismo (accessed on 9 July 2020).
- Boyce, M.S.; Vernier, P.R.; Nielsen, S.E.; Schmiegelow, F.K. Evaluating resource selection functions. Ecol. Model.
**2002**, 157, 281–300. [Google Scholar] [CrossRef] [Green Version] - Hirzel, A.H.; Le Lay, G.; Helfer, V.; Randin, C.; Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Model.
**2006**, 199, 142–152. [Google Scholar] [CrossRef] - Di Cola, V.; Broennimann, O.; Petitpierre, B.; Breiner, F.; D’Amen, M.; Randin, C.; Engler, R.; Pottier, J.; Pio, D.; Dubuis, A.; et al. ecospat: An R package to support spatial analyses and modeling of species niches and distributions. Ecography
**2017**, 40, 774–787. [Google Scholar] [CrossRef] - Lobo, J.M.; Jiménez-Valverde, A.; Real, R. AUC: A misleading measure of the performance of predictive distribution models. Glob. Ecol. Biogeogr.
**2008**, 17, 145–151. [Google Scholar] [CrossRef] - Petitpierre, B.; Kueffer, C.; Broennimann, O.; Randin, C.; Daehler, C.; Guisan, A. Climatic niche shifts are rare among terrestrial plant invaders. Science
**2012**, 335, 1344–1348. [Google Scholar] [CrossRef] [Green Version] - Broennimann, O.; Fitzpatrick, M.C.; Pearman, P.B.; Petitpierre, B.; Pellissier, L.; Yoccoz, N.; Thuiller, W.; Fortin, M.-J.; Randin, C.; Zimmermann, N.E.; et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr.
**2011**, 21, 481–497. [Google Scholar] [CrossRef] [Green Version] - Warren, D.; Glor, R.E.; Turelli, M. Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution
**2008**, 62, 2868–2883. [Google Scholar] [CrossRef] - Manly, B.F. Multivariate Statistical Methods, A Primer, 2nd ed.; Chapman and Hall: London, UK, 1994. [Google Scholar]
- Zar, J.H. Biostatistical Analysis; Prentice Hall: New Jersey, NJ, USA, 2010. [Google Scholar]
- Feltz, C.J.; Miller, G.E. An asymptotic test for the equality of coefficients of variation from k population. Stat. Med.
**1996**, 15, 647–658. [Google Scholar] [CrossRef] - Hothorn, T.; Bretz, F.; Westfall, P. Simultaneous inference in general parametric models. Biom. J.
**2008**, 50, 346–363. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Anonymous. The R Project for Statistical Computing. Available online: http://www.r-project.org/ (accessed on 13 February 2012).
- RStudio is an Integrated Development Environment (IDE) for R Language. Available online: https://www.rstudio.com (accessed on 9 July 2020).
- Tuniyev, B.S.; Lotiev, K.Y.; Tuniyev, S.B.; Gabaev, V.N.; Kidov, A.A. Amphibians and reptiles of South Ossetia. Nat. Conserv. Res.
**2017**, 2, 1–23. [Google Scholar] [CrossRef] [Green Version] - Tuniyev, B.S.; Tuniyev, S.B.; Avci, A.; Ilgaz, Ç. Herpetological studies in eastern and north-eastern Turkey. Curr. Herpetol.
**2014**, 14, 44–53. [Google Scholar] - Breiner, F.; Guisan, A.; Bergamini, A.; Nobis, M.P. Overcoming limitations of modelling rare species by using ensembles of small models. Methods Ecol. Evol.
**2015**, 6, 1210–1218. [Google Scholar] [CrossRef] - Darevsky, I.S.; Shcherbak, N.N. Acclimatization of parthenogenetic lizards in Ukraine. Priroda
**1967**, 3, 93–94. [Google Scholar] - Darevsky, I.S.; Kan, N.G.; Ryabinina, N.L.; Martirosyan, I.A.; Tokarskaya, O.N.; Grechko, V.V.; Shcherbak, N.N.; Danielyan, F.D.; Ryskov, A.P. Biochemical, molecular, and genetic characteristics of parthenogenetic lizards Lacerta armeniaca (Mehely), introduced from Armenia to Ukraine. Dokl Akad Nauk.
**1998**, 363, 846–848. [Google Scholar] - Dotsenko, I.B.; Peskov, V.N.; Miropolskaya, M.V. Comparative analysis of genus Darevskia rock lizards external morphology from the territory of Ukraine, and the species belonging of them. Proc. Zool. Mus.
**2008–2009**, 40, 130–142. [Google Scholar] - Darevsky, I.S.; Kulikova, V.N. Natürliche Parthenogenese in der polymorphen Gruppe der Kaukasischen Felseidechse (Lacerta saxicola Eversmann). Zool. Jahrb. Syst.
**1961**, 89, 119–176. [Google Scholar] - Parker, E.D.; Selander, R.K.; Hudson, R.O.; Lester, L.J. Genetic diversity in colonizing parthenogenetic cockroaches. Evolution
**1977**, 31, 836–842. [Google Scholar] [CrossRef] - Lynch, M.; Bürger, R.; Butcher, D.; Gabriel, W. The Mutational meltdown in asexual populations. J. Hered.
**1993**, 84, 339–344. [Google Scholar] [CrossRef] [Green Version] - Nekrasova, O.D.; Kostiushyn, V.A. Current Distribution of the Introduced Rock Lizards of the Darevskia (Saxicola) Complex (Sauria, Lacertidae, Darevskia) in Zhytomyr Region (Ukraine). Vestnik Zool.
**2016**, 50, 225–230. [Google Scholar] [CrossRef] - Vrijenhoek, R.C. Factors affecting clonal diversity and coexistence. Am. Zool.
**1979**, 19, 787–797. [Google Scholar] [CrossRef] [Green Version] - Vrijenhoek, R.C. Ecological Differentiation Among Clones: The Frozen Niche Variation Model. In Population Biology and Evolution; Springer: Berlin/Heidelberg, Germany, 1984; pp. 217–231. [Google Scholar]
- Weeks, S.C. The effects of recurrent clonal formation on clonal invasion patterns and sexual persistence: A monte carlo simulation of the frozen niche-variation model. Am. Nat.
**1993**, 141, 409–427. [Google Scholar] [CrossRef] [PubMed] - Girnyk, A.E.; Vergun, A.A.; Semyenova, S.K.; Guliaev, A.; Arakelyan, M.; Danielyan, F.D.; Martirosyan, I.A.; Murphy, R.W.; Ryskov, A. Multiple interspecific hybridization and microsatellite mutations provide clonal diversity in the parthenogenetic rock lizard Darevskia armeniaca. BMC Genom.
**2018**, 19, 979. [Google Scholar] [CrossRef] [PubMed] - Shine, R. Seasonal shifts in nest temperature can modify the phenotypes of hatchling lizards, regardless of overall mean incubation temperature. Funct. Ecol.
**2004**, 18, 43–49. [Google Scholar] [CrossRef] [Green Version] - Nei, M. The new mutation theory of phenotypic evolution. Proc. Natl. Acad. Sci. USA
**2007**, 104, 12235–12242. [Google Scholar] [CrossRef] [Green Version] - Dessauer, H.C.; Cole, C.J. Diversity between and within Nominal Forms of Unisexual Teiid Lizards. In Evolution and Ecology of Unisexual Vertebrates; Dawley, R.M., Bogart, J.P., Eds.; New York State Museum Bulletin: Albany, NY, USA, 1989; Volume 466, pp. 49–71. [Google Scholar]
- Moritz, C.; Uzzell, T.; Spolsky, C.; Hotz, H.; Darevsky, I.; Kupriyanova, L.; Danielyan, F. The material ancestry and approximate age of parthenogenetic species of Caucasian rock lizards (Lacerta: Lacertidae). Genetica
**1992**, 87, 53–62. [Google Scholar] [CrossRef]

**Figure 2.**Niche overlaps of D. dahli, D. portschinskii and D. mixta in multidimensional space of predictor variables. Panels (

**a**,

**b**) represent the niche overlap between D. dahli and D. portschinskii along the two first axes of the PCA; (

**c**,

**d**) represent the niche overlap between D. dahli and D. mixta. Shaded areas show the density of the occurrences of D. dahli (

**a**,

**c**), D. portschinskii (

**b**) and D. mixta (

**d**). The solid and dashed lines illustrate, respectively, 100% and 90% of the available (background) environment.

**Figure 3.**The positions of the centroids of the ecological niches of the rock lizards along the environmental gradients with 95% confidence intervals of Tukey HSD. The GLM ANOVA tested the main factor effects of the lizards—(

**a**) F = 46.3; p <<0.01; (

**b**) F = 44.8; p << 0.01; (

**c**) F = 16.5, p << 0.01; (

**d**) F = 22.58; p << 0.01; (

**e**) F = 270.31, p << 0.01; (

**f**) F = 295.6; p << 0.01; (

**g**) F = 66.6; p << 0.01; (

**h**) F = 16.9; p << 0.01; (

**i**) F = 17.6; p <<0.001; (

**j**) F = 22.49; p << 0.01 (F is Fisher’s test; p value is given for the factor effects). Absence of difference between means using Post hoc Tukey HSD test are marked by * (p-values of the all comparison pairs are presented in Figure S9).

**Figure 4.**The percentage of preferred vegetation types with 95% Wald’s confidence intervals. A multiple comparison was performed using the Chi-square (a: 13.4, DF = 2, p = 0.001; b: 17.7; DF = 2, p << 0.001; c: 5.9, DF = 2, p = 0.05; d: 5.84, DF = 2, p = 0.05) and Tukey’s Post hoc tests. Absence of significant differences between the means was designated *.

**Table 1.**The list of predictor variables selected for building SDM of D. dahli, D. portschinskii and D. mixta, where R

_{P}is the largest value of the Pearson’s correlation coefficient; R

^{2}is the coefficient of determination of a linear regression of each predictor variable on all other predictor variables, VIF is Variance Inflation Factor.

Variable | Code | R^{2} | VIF |
---|---|---|---|

D. dahli, R_{P} = 0.63 | |||

Solar irradiation (kJ m^{−2} day^{−1}) | C_SRad | 0.72 | 3.53 |

Precipitation in warmest quarter (mm) | C_PWarmQ | 0.63 | 2.69 |

Elevation (m) | T_EL | 0.42 | 1.72 |

Isothermality, % | C_ISOT | 0.26 | 1.35 |

Distance to road (m) | L_DHW | 0.09 | 1.1 |

D. portschinskii, R_{P} = 0.72 | |||

Solar irradiation (kJ m^{−2} day^{−1}) | C_SRad | 0.86 | 7.28 |

Elevation (m) | T_EL | 0.77 | 4.43 |

Mean temperature in driest quarter (°C) | C_MeanTDrQ | 0.77 | 4.27 |

Precipitation in warmest quarter (mm) | C_PWarmQ | 0.76 | 4.18 |

Annual temperature range (°C) | C_TAnR | 0.72 | 3.56 |

Precipitation seasonality (coefficient of variation) (%) | C_PCoefVar | 0.56 | 2.28 |

Isothermality, % | C_ISOT | 0.56 | 2.27 |

Vegetation type | L_VEG | 0.56 | 0.44 |

Distance to road (m) | L_DHW | 0.12 | 1.14 |

D. mixta, R_{P} = 0.69 | |||

Solar irradiation (kJ m^{−2} day^{−1}) | C_Srad | 0.76 | 4.13 |

Precipitation in warmest quarter | C_PWarmQ | 0.65 | 2.87 |

Precipitation seasonality (coefficient of variation) (%) | C_PCoefVar | 0.54 | 2.16 |

Elevation (m) | T_EL | 0.47 | 1.9 |

Vegetation type | L_VEG | 0.41 | 1.7 |

Distance to road (m) | L_DHW | 0.07 | 1.08 |

**Table 2.**Table of contribution of the most important variables obtained by Maxent SDMs. Significant contributions of variables are bolded, where PC is a percentage of contribution, PI is permutation importance.

Predictor Variables | D. dahli | D. portschinskii | D. mixta | |||
---|---|---|---|---|---|---|

PC | PI | PC | PI | PC | PI | |

C_ISOT | 24.4 | 10.4 | 12.6 | 21.9 | 0.3 | 1 |

C_TAnR | 0.1 | 0.1 | 1.5 | 5.6 | 0.8 | 0.7 |

C_MeanTDrQ | 0.2 | 0 | 9.1 | 8.6 | 0.1 | 0 |

C_PCoefVar | 1.7 | 0.8 | 3.9 | 5.3 | 36.8 | 44.5 |

C_PWarmQ | 30 | 50.2 | 32.7 | 22.3 | 30.1 | 20.4 |

C_SRad | 12.4 | 22.7 | 17.8 | 26.4 | 8.7 | 17.4 |

T_EL | 13.6 | 13.7 | 6.6 | 1.8 | 4.9 | 9.1 |

L_DHW | 9 | 0.1 | 5.4 | 0.1 | 0.2 | 0.1 |

L_VEG | 0.2 | 0.3 | 5.1 | 1 | 8.3 | 0.8 |

Boyce index (±SE) | 0.95(±0.004) | 0.93 (±0.004) | 0.94 (±0.003) |

**Table 3.**Niche overlap assessed using Schoener’s D indices between D. dahli and parental species (D. portschinskii and D. mixta) ranges. Where E is expansion, S is stability, U is unfilling, p-values of the niche similarity test are given for a pairwise comparison.

Parental Species | Schoener’s D Index | p-Value | E | S | U |
---|---|---|---|---|---|

D. mixta | 0.22 | 0.09 | 0.12 | 0.88 | 0.57 |

D. portschinskii | 0.72 | 0.009 | 0.02 | 0.98 | 0.06 |

© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

## Share and Cite

**MDPI and ACS Style**

Petrosyan, V.; Osipov, F.; Bobrov, V.; Dergunova, N.; Omelchenko, A.; Varshavskiy, A.; Danielyan, F.; Arakelyan, M.
Species Distribution Models and Niche Partitioning among Unisexual *Darevskia dahli* and Its Parental Bisexual (*D. portschinskii*, *D. mixta*) Rock Lizards in the Caucasus. *Mathematics* **2020**, *8*, 1329.
https://doi.org/10.3390/math8081329

**AMA Style**

Petrosyan V, Osipov F, Bobrov V, Dergunova N, Omelchenko A, Varshavskiy A, Danielyan F, Arakelyan M.
Species Distribution Models and Niche Partitioning among Unisexual *Darevskia dahli* and Its Parental Bisexual (*D. portschinskii*, *D. mixta*) Rock Lizards in the Caucasus. *Mathematics*. 2020; 8(8):1329.
https://doi.org/10.3390/math8081329

**Chicago/Turabian Style**

Petrosyan, Varos, Fedor Osipov, Vladimir Bobrov, Natalia Dergunova, Andrey Omelchenko, Alexander Varshavskiy, Felix Danielyan, and Marine Arakelyan.
2020. "Species Distribution Models and Niche Partitioning among Unisexual *Darevskia dahli* and Its Parental Bisexual (*D. portschinskii*, *D. mixta*) Rock Lizards in the Caucasus" *Mathematics* 8, no. 8: 1329.
https://doi.org/10.3390/math8081329