Introduction

Exploring historical and current drivers of species richness can inform on how those gradients might be reshaped in the future1,2,3. Present environmental variables including climate, habitat heterogeneity, productivity represent important drivers of species distribution and diversity4,5,6,7. Diversity of present assemblages is not always in equilibrium with current climate. Thus, past climate changes may better reflect species richness2 or global endemism than current climate8,9. Beyond the Quaternary, mountain uplifting might also be associated to the formation of biodiversity gradients, sha** an association between habitat heterogeneity and species richness10,11. Together, it appears there is no single driver of species distribution across broad geographical range and species distributional patterns are shaped by the interplay between different historical and ecological factors2,3,11,12,13. The interplay between contemporary and historical variables in sha** biodiversity might vary between ecosystems types, biogeographic regions and taxonomic groups2,3,11,13.

With ca. 10,970 known species, reptiles are a highly diverse group of vertebrates14, but they are generally less studied compared to other vertebrate groups such as birds and mammals5,15,16. Reptiles are characterized by low dispersal ability and narrow ecological niches17. Thus, they are suitable biological models to assess the role of historical factors in sha** spatial distribution of biodiversity18,19. Global coarse scale distribution maps indicate that reptile richness is highest in pantropical including Central America, South America, south of Africa, Southeast Asia and Australia20. But some regions are less known than others, and lack high resolution distribution information. However, lizard richness is somehow different from reptile as their numbers are found to be maximum in both tropical and arid regions and reach a peak in Australia20. In particular, the highest proportions of threatened and Data Deficient21 reptiles are occurring in tropical areas20. Agriculture, biological resource use and urban development are the most important threats to reptile worldwide20.

Climate and topography are introduced as the most important contemporary determinants of reptile richness at global and regional scales22,23,24,25. In fact, reptile richness is highest in areas which characterized with high temperature and high topographic heterogeneity22,23,24,25. But the variables associated with the richness of reptile at regional scale in subtropical and desert areas were less investigated. While, reptiles have previously been the targets of richness map**22,26,27,28, the influence of historical processes on their richness in southwest Asia was rarely quantified29,30,31. Among the historical factors, the influence of Quaternary climatic oscillations and mountains uplifting was observed on individual species, using genetic data and species distribution modelling32,33,34,35,36,37.

Iran is one of the biologically diverse countries in southwest Asia38, it is home to ca. 241 reptile species, of which ca. 71 are endemic to the country39. The country is a suitable place to test the effects of historical events on distribution of biodiversity. Iran’s current topography was shaped by uplifting of the different mountain ranges, which facilitated species diversification by providing new unoccupied niches34,35,37,40. The country also experienced several glacial periods41, which influenced reptile distribution36,42,43. Despite the fact that natural history studies have been initiated over 300 years ago in Iran38, the distribution and ecology of many species occupying that region remain poorly known38,44,45. Recent discoveries of novel lizards and snakes in Iran suggest that the biodiversity of Iran is still poorly explored and should receive further attention46,47. Distributions of some species like Heremites vittatus, Saara loricate and Phrynocephalus scutellatus were mapped using species distribution modeling45,48,49. Based on these studies, climate was the most important determinant of reptile distribution in Iran. Climate was also identified as a most influential variable in sha** reptile richness in the country30. However, there is a knowledge gap in the ecology and distribution of lizard species in Iran44,45,49. In this study, we mapped the species distribution of all lizards in Iran and quantified reptile richness. We associated species richness to ecological drivers of reptile distributions in Iran30, but considered in addition Quaternary climatic oscillations and mountains uplifting events. We had the following expectations:

  1. 1.

    The age of mountain uplifting have shaped topography as well as Quaternary glaciation should be associated to the present diversity of lizard species in Iran.

  2. 2.

    Among the ecological factors climatic variables are more influential in sha** lizard richness patterns.

  3. 3.

    Because nocturnal and diurnal species have different natural history, their richness is expected to be shaped by different historical and ecological variables.

Results

Species richness patterns

The 171 lizard species belonged to ten families and 47 genera. Family Gekkonidae and genus Eremias were most divers family and genus in Iran with 51 and 20 species respectively. Of 171 recognized lizard species in Iran 101 species (59.06%) were diurnal, 70 species nocturnal (40.93%) and 62 species endemic (36.25%).

The map** of the distribution of 171 lizard species showed that Western Zagros Mountains with 37 species, north western parts of Central Iranian Plateau with 30 species and north eastern parts with 28 species have the highest lizard richness in Iran (Fig. 1a). In contrast, northern parts of the country, Kopet-Dagh Mountains and Elburz Mountains with 2–14 species have relatively lower number of species. For diurnal species, Zagros Mountains with 22 species, north eastern and north western parts of Central Iranian Plateau with 23 species show the highest number of species (Fig. 1b). Nocturnal species hotspots occur in Western Zagros Mountains with 17 species, north of Persian Gulf and Oman Sea with 13 species, while we found that central parts of Iran with 1–6 species, Kopet-Dagh Mountains and Elburz Mountains with 0–4 species have much lower number of nocturnal species across the country (Fig. 1c). Results showed that hotspots of all lizards contain 37 species, diurnal lizard 23 and nocturnal lizards 17 species. Lut Desert contains lowest number of species for the three groups.

Figure 1
figure 1

Richness map of all (a) diurnal (b) and nocturnal (c) lizards in Iran. All species richness range from 0 to 37, diurnal from 0 to 23 and nocturnal from 0 to 17. Maps were generated using QGIS 3.4.1 (https://www.qgis.org).

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Drivers of lizard richness in Iran

We found that all historical and ecological variables are significantly correlated with lizard richness (Table 1). We determined which variable explained highest proportion of variance among ecological and historical variable. Results showed that annual mean temperature explained largest variance for all species (10%) and nocturnal species (31%). For diurnal species, velocity of temperature shows strongest effect in explaining variance in observed richness pattern (26%). The distribution of lizard richness has a positive relationship with annual mean temperature and the number of species increases with higher mean temperatures for the three groups (all species, diurnal and nocturnal). Topographic heterogeneity is positively correlated with lizard species richness but NDVI was negatively correlated with richness for the three groups. Richness is negatively correlated with precipitation for the three groups. Temperature change velocity is positively associated with higher number of species for all lizards, diurnal and nocturnal lizards and maximum number of species occur in areas with moderate level of temperature change velocity.

Table 1 Results of generalized linear model with quasi-Poisson distribution.
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Discussion

We mapped the richness of all recognized lizard species in Iran, using distribution data of 171 lizard species and documented pronounced gradients of species richness, which were different between nocturnal and diurnal species. The Western Zagros Mountains, north eastern and north western parts of Central Iranian Plateau have the highest number of species, with a peak specifically in the Zagros Mountains.

Climatic variables were identified as the important drivers of reptile distribution around the globe5,22. Our results supported previous effects of climate and showed that temperature was the best explaining variable for richness of all and nocturnal species, while temperature change velocity explained highest fraction of variation in diurnal species richness. Hosseinzadeh, et al.30 also showed that temperature is the most important predictor of reptile distribution in Iran. A positive association was frequently reported for reptile richness and temperature around the world50. Body temperature, which is the most important ecophysiological variable affecting the performance of reptiles, is regulated by ambient energy input51. Annual mean temperature is an indicator of ambient energy input52 and it is often used as a measure of environmental energy53. Thus, areas with higher temperature and consequently higher ambient energy can support more species52,53. This is why a positive association was found between lizard richness and temperature in all three groups. In agreement with our expectations, nocturnal and diurnal lizard richness was shaped by different contemporary and historical variables. Moreover, we found that areas which receive less precipitation have more lizard species, while in other group of reptiles, such as turtles, richness may show the opposite response and increase with precipitation54,55. Nocturnal lizards are richest in the tropics and deserts, and their richness decreases with latitude56. Nocturnal lizards, especially those of the families Gekkonidae, Sphaerodactylidae and Phyllodactylidae are more divers in the south of Iran than the rest of the country38,39. Annual mean temperature is increased toward southern Iran, that could be linked to the increased diversity of nocturnal lizards. In warm environments, the hot days increases the cost of diurnal activity, whereas nocturnal activity provides a shelter from these extreme conditions, for e.g. feeding and reproduction.

Quaternary climatic change was associated with distribution biodiversity in high latitude57. Our results show that past climate change also played important role in sha** biodiversity distribution in lower latitude as well. During the ice ages, mountains of Iran were covered by snow and ice line and snow line was much lower than what we see today41. So reptiles of Iran have undergone several cycles of range expansion–contraction due to the climate fluctuations which in turn shaped their current distribution36,42,43. We found that temperature change velocity was the most important variable in explaining variation in diurnal species richness and the second most important predictor of all lizard richness. Past climate change was not important in sha** nocturnal species richness because their richness reach a peak at south of Iran38,39 which was not influenced by past climatic changes41.

Our results agree with previous studies, which have shown that past climate is a major determinant of reptile richness13,31. For example, Araújo, et al.13 showed that past climate played an important role in sha** large-scale species richness patterns of reptiles and amphibians across Europe. In another study Ficetola et al. 31 quantified the importance of past climate on reptiles of the Western Palearctic. In both studies, reptile richness and endemism were highest in areas with high climate stability, low climate change velocity. Our findings showed that lizard richness was positively associated with temperature change velocity, areas with moderate climate change velocity were correlated with maximum number of species. Our finding is in line with previous studies which highlighted the role of Quaternary climatic oscillations on Iran’s biodiversity using genetic data and species distribution modeling34,42,43. Zagros Mountains which contain highest number of species was a refugium for several taxonomic groups during past climatic oscillations including reptiles34,42,43,58, amphibians59,60 birds61,62, and mammals63,64,65.

As pointed by Wines and Graham66, there might be strong correlation between species richness and some environmental variables but environmental variables (in our case temperature) cannot change the number of species in particular region66. Species richness pattern linked to processes like speciation, dispersal and extinction66,67. Zagros uplifting caused speciation by splitting populations of species and by providing unoccupied niches for species of the genus Eremias, Mesalina, Timon and Sarra32,35,38,68. Climatic changes also strongly influenced lizard distribution pattern and played important role in their isolations and dispersal in Zagros region34,69. There are some sky island species which remained in climatic refugia in Zagros Mountains like Iranolacerta brandtii and Iranolacerta zagrosica during past climatic oscillations34. In addition, Zagros acted as dispersal barrier and known as dispersal corridor for different species of lizards38,69,70. According to our knowledge, there is not any specific driver of extinction of lizard in the area. Thus, among the three main processes which are linked to species richness in each region, speciation and dispersal due to Zagros uplifting and past climatic fluctuations, are the main drivers of lizard richness patterns (high richness in Zagros region).

In this study, Zagros Mountains were identified as hotspot of lizard richness in Iran. This region was also identified as hotspot of biodiversity for mammals and plants in the country7,71. Our analyses indicate that the Zagros Mountains are a region of moderate climate stability and high topographic heterogeneity, providing a high diversity of climatic niches. Furthermore, the Zagros Mountains are located in the Irano-Anatolian biodiversity hotspot72, showing that there are local hotspots of biodiversity nested within regional biodiversity hotspots7. Zagros Mountains were also identified as an endemism area for reptiles of the Western Palearctic31. Beside reptiles, there are some high prioritized species for conservation such as the Luristan newt (Neurergus kaiseri), which was ranked as 45th among the world’s 100 top priority amphibian species73. This combination of high diversity and endemism makes Zagros Mountains a most valuable target for conservation of biodiversity in Iran.

Conclusion

Altogether, our results suggest that lizard richness can be explained by current and past climate in Iran. There are studies which quantified the role of ecological factors on reptile richness in southwest Asia (for instance29,30,31), while historical drivers of reptile richness remain poorly understood31. For better understanding the drivers of current species distribution, we need to look at past and investigate the role of historical factors on species distribution. This study took in to account both historical and ecological factors effects on the distribution patterns of 171 lizard species in Iran. Our findings support the fact that there is no single driver for biodiversity distribution and there is always a set of ecological and historical factors sha** species richness3,11,12,74. Since lizard richness is strongly associated with climate we speculate that lizard diversity and distribution will be affected by future climatic changes. Documented patterns of our study provide a baseline for understanding the potential effect of ongoing climate change on lizards in Iran.

Methods

Study area

Iran covers 164.8 million hectares, located in the Palearctic region at the crossroads of three biogeographic realms; Afrotropic, Palearctic and Indomalaya. Iran hosts over ca. 8000 plant species75,76 and more than 1214 vertebrate species of which many are endemic to the country38,39,71,77. The elevation ranges from − 26 to 5770 m and a large fraction of the country has an elevation above 1200 m. Iran’s current topography (Fig. 2) was shaped mainly via tectonic activities of Arabia–Eurasia continent collision78. This collision generated in around early Miocene, approximately 19 Mya79,80 and the last mass tectonic event in this zone occurred in late Miocene and the beginning of the Pliocene, 5 Mya, when progressive anticlockwise rotation of the Arabian Peninsula associated with the formation of the Red Sea and Gulf of Aden81. The collision of Arabia – Eurasia continents resulted in multi stage uplift of the Zagros Mountains, as well as the uplift of the whole plateau. The Elburz Mountains in northern Iran are stretching from west to east at the southern coast of the Caspian Sea and form the northern border of the Iranian Plateau. They are more than 1000 km long and the width varies from 30 to 130 km in different parts. The northern slopes of Elburz Mountains are covered by Hyrcanian forests. Kopet Dagh Mountains is a large mountain range (about 650 kms along) which is located in the northeast of Iran between Iran and Turkmenistan, stretching from near the Caspian Sea to the Harirud River. Zagros Mountains form the western and south-western borders of the Iranian Plateau, covering 1500 km from Lake Van in Turkish Kurdistan to south-eastern Iran. Iran has two well-known deserts, the Kavir Desert and the Lut Desert which are among the hottest areas in the world, located in Iran's central plateau. The Quaternary has been a period of global climate oscillation and several Quaternary climatic changes occurred in Iran, also on the dry Iranian highlands82. The most recent glaciation, termed the Riss-Würm, reached its maximum about 18,000–21,000 years ago, and subsequently replaced by Holocene Climatic Optimum (HGO), 9000–5000 years ago83,84. During this period, in northern and western Iran climate changed between dry and cold climatic conditions during the glaciation and moist and warm conditions during the interglacials82,83,84.

Figure 2
figure 2

A topographic overview of Iran with its major geomorphological features. Map was generated using QGIS 3.4.1 (https://www.qgis.org).

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Distribution points

Distribution records of all 171 recognised lizard species of Iran (see Appendix S1 for annotated checklist of lizards of Iran) were collected from multiple sources; (1) through opportunistic observations and long term own and other colleagues fieldworks from 2009 to 2020 (Using random field surveys different habitat types within the county were investigated (See Appendix S2 Figs. S1–S36 for examples habitats surveyed during fieldworks and observed lizard species in each habitat)), (2) published papers and books (see Appendix S3) and (3) from the Global Biodiversity Information Facility (GBIF: https://www.gbif.org/). Observed lizards were identified following Anderson38, Rastegar-Pouyani et al.39 and Narabadi et al.85. In total, we collected 8620 distribution points from these sources. Since our distribution records come from multiple sources, we carefully checked distribution data, removing duplicate records and distribution records lacking geographic coordinates. Reliability of all 171 lizard species’ distribution records was examined by map** each species records separately in DIVA-GIS 7.586. We also thinned distribution records of each species to 1 km reduce clustering. Finally, we used 6245 species presence records.

Environmental variables

We selected seven variables (Table 2) related to climate: topography, the normalized difference vegetation index (NDVI), climate change velocity and geology which we expected to be important in sha** distribution of reptiles22,23,24,30,32,33,34,35,3845,48,49,87. To quantify climate effect on reptile distribution, we used temperature and annual precipitation13. Current climate data was downloaded from WorldClim (www.worldclim.org). We quantified topographic heterogeneity by measuring the standard deviation of elevation values in area grid cells of 1 km from a 90 m resolution88. Elevation layer obtained from the Shuttle Radar Topography Mission (SRTM) elevation model89. The climate change velocity was calculated following Sandel et al.9. We used temperate and precipitation data of current climatic conditions (1970–2000) and Last Glacial Maximum (LGM; 21,000 years before present) to calculate climate change velocity as the rate of climate change in time divided by the local climate change in space. Climate change velocity is a measurement for long-time climate variability9,90 and it shows the direction and rate at which organisms must have moved to maintain a given climate under climate change9,91. In previous research, climate change velocity was identified to be strongly associated with species richness and endemism at regional and global scales9,90,92. LGM data were obtained from CCSM4 and MIROC 3.2 (averaged values) downloaded from WorldClim (www.worldclim.org). Temperature and precipitation change velocity were calculated in R 3.393 environment using the packages raster94, gdistance95 matrixStats96 and SDMTools97. To explore the possible role of mountains uplifting on lizard richness we assembled information on uplift age of each major mountain range based on the available literatures78,98,99,100,101,102, then combined this information in a raster layer containing uplift age of the various mountain ranges in Iran. The layer with uplifting age of mountain ranges was created using QGIS 3.4.1103.To avoid collinearity among variables a variance inflation factor (VIF104) was calculated for the variables using the ‘vifstep’ function in the ‘usdm’ package105 in R 3.393 environment and results showed that collinearity among variables is low (VIF values: annual mean temperature = 1.356, annual mean precipitation = 3.86, topographic heterogeneity = 1.614, NDVI = 3.041, temperature change velocity = 1.185, precipitation change velocity = 1.153, mountains uplifting = 1.056).

Table 2 List of ecological and historical predictors used to explore drivers of lizard richness.
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Species richness map**

We followed the method applied by Pellissier et al.11 and Albouy et al.109 to map species ranges and then multiply them to create lizard richness in Iran. This method uses species occurrence records, border of biomes (Fig. 3) of the study area and a climatic layer (here we used annual mean temperature an important factor in sha** reptile distribution) to create species range maps. We separated Iran into six biomes based on the World Wildlife Fund (WWF) Terrestrial Ecoregions including the following; Temperate Broadleaf and Mixed Forests, Temperate Grasslands, Savannahs and Shrublands, Temperate Conifer Forests, Montane grasslands and shrublands, and Deserts and Xeric Shrublands110. This approach goes through several steps to map species distribution; first, we created a convex hull polygon around all the observations within one bioregion. If there is only one observation in a bioregion, it will create a buffer around it of 50 km. Then to remove potential outliers, we quantified the 2.5th and 97.5th temperature values from the occurrence, where a species is found. We removed areas that are outside those temperature conditions. Together, we created range maps of all 171 lizard species, and we stacked the species distribution maps into species richness using raster package94 in R environment93 to create three richness maps; all lizards, diurnal lizards and nocturnal lizards.

Figure 3
figure 3

Iran’s terrestrial biomes110, together with representative lizards species occur in Temperate Broadleaf and Mixed Forests: 2.1 Paralaudakia microlepis, 2.2 Timon kurdistanicus, 2.3 Anguis colchica, 2.4 Pseudopus apodus; Temperate Grasslands, Savannahs, and Shrublands: 2.5 Lacerta media; Temperate Conifer Forests: 2.6 Paralaudakia caucasia, 2.7 Eremias papenfussi; Montane grasslands and shrublands: 2.8 Eremias kopetdaghica, 2.9 Darevskia kopetdaghica, 2.10 Eremias isfahanica; Deserts and Xeric Shrublands: 2.11 Eremias fasciata, 2.12 Teratoscincus scincus, 2.13 Phrynocephalus mystaceus, 2.14 Varanus griseus 2.15 Eremias persica. Map was generated using QGIS 3.4.1 (https://www.qgis.org).

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Statistical analyses

We fitted a generalized linear model (GLM) with quasi-Poisson distribution in order to explore the relationship between reptile richness (number of species in each raster pixel) and the different historical and ecological factors. We estimated the Akaike information criterion values (AIC) and computed the explained deviance for each predictor separately and in combination for full model using the ‘ecospat.adj.D2.glm’ function in the R‐package ‘ecospat’111. Nocturnal and diurnal species have different natural and evolutionary history and their distribution patterns are different in Iran38,44. For example, most of the nocturnal species are occur in south of Iran which characterized with high temperature and more stable climate since LGM68. Thus, nocturnal and diurnal lizard distribution is most likely affected by different ecological and historical variables. So, we did the analysis for all lizard, diurnal and nocturnal separately to test whether there are different drivers for diurnal and nocturnal species. Analyses were carried out in R 3.393.