Acanthodactylus micropholis Heidari, Rastegar-Pouyani, Rastegar-Pouyani & Rajabizadeh, 2013 and A. khamirensis Blanford, 1874 are genetically and morphologically distinct, but their ecological differentiation has not previously been evaluated. The ecological niche models of these two sister species Acanthodactylus were reconstructed using climate and geographical data. Species distribution modeling for A. micropholis and A. khamirensis was used to make predictions and showed that most parts of southern and southeastern Iran are suitable for the distribution of both species. Habitat suitability was mostly dependent upon minimum temperature of the coldest month and seasonal precipitation for A. micropholis and A. khamirensis, respectively. Niche similarity tests (niche overlap and identity tests) were performed to evaluate species differentiation based on the ecological species criterion. Our results indicate that both species have different ecological niches and are significantly separated from each other. Therefore, our study corroborates previous analyses based on molecular and morphological evidences that suggested that A. micropholis and A. khamirensis were valid species.

Ecological species concept, fringed-toed lizard, Iranian Plateau, precipitation, temperature

Species delimitation is a great challenge in biology (Wiens 2007), because biologists base it on a variety of different criteria, such as morphology, phylogeny, anatomy, acoustic, biology and ecology (De Queiroz 2007). Different species are adapted to their habitats and are also isolated from each other by post- or prezygotic barriers (the biological species concept) (Mayr 1978). In some cases, the biological species concept is insufficient to describe the true relationship between species, meaning that more criteria are needed to confirm the separation of the gene pool of a given species from other species (Templeton 1989, Jones 2003, Baker and Bradley 2006). Recently, new methods in molecular phylogeny, morphology, and ecology have been developed that aid in greater clarification of species separation (Schlick-Steiner et al. 2010, Fujita et al. 2012). According to the ecological criterion, each species occupies its own ecological niche space and cannot allow other species to enter the space (Van Valen 1976). To examine whether species occupy distinct niche spaces, ecological niche models (ENMs) have been used in which bioclimatic variables are used to compare species spaces and to find the degree of niche overlap between them (Peterson et al. 1999, Wiens 2004, Raxworthy et al. 2007, Barve et al. 2011). Speciation occurs when two populations are isolated from each other genetically and ecologically, after which they consequently develop morphological differentiation (Wiens 2004). Because morphological differentiation appears at the final stage, it is important to evaluate molecular and ecological differentiation as well.

Lacertid lizards of the genus Acanthodactylus have a wide distribution range from North Africa through the Middle East and Iranian Plateau (Tamar et al. 2016). So far, eight species of this genus have been recorded from Iran (Safaei-Mahroo et al. 2015). Recently, the genus has been revised using molecular phylogeny (Heidari et al. 2014) and a new species, A. khamirensis, was described as belonging to the “micropholis” species complex (Heidari et al. 2013). In both species description papers, morphological and molecular markers confirmed the specific level of the newly described species. However, it is still important to examine the ecological niche separation of these lizards for more confirmation.

In this study, the ecological niche differentiation between two species (Acanthodactylus micropholis Blanford, 1874 and A. khamirensis Heidari, Rastegar-Pouyani, Rastegar-Pouyani & Rajabizadeh, 2013) was examined. Also, modeling was used to predict the potential distribution of both species in south of Iran and the degree of niche space overlap between them. Finally, we discuss important abiotic factors (temperature and precipitation) affecting geographic isolation and niche differentiation based upon ecological niche modeling.

All occurrence records of both species were obtained from the literature (Heidari et al. 2013, 2014, Šmid et al. 2014). In total, 45 presence records belonging to both species (nine records for A. khamirensis and 35 records for A. micropholis) (Appendix 1) were used. In total, 19 bioclimatic variables were downloaded from the WorldClim website (Hijmans et al. 2005) in 30 arc-second resolution. All layers were clipped using ArcGIS 10.3 (ESRI) for the Iranian boundaries. To elucidate the autocorrelation relationship between variables, Openmodeller v. 1.0.7 (de Souza Muñoz et al. 2011) was employed. Relevant grid values for each variable were extracted and imported into SPSS v. 16.0, then analyzed for the bivariate-correlation Pearson coefficient. Variable pairs with correlation ≥ 0.7 were removed from the analyses. Finally, six bioclimatic variables were selected for analyses as follows: BIO3 (Isothermality); BIO6 (Minimum Temperature of Coldest Month); BIO9 (Mean Temperature of Driest Quarter); BIO12 (Annual Precipitation); BIO15 (Precipitation Seasonality); BIO17 (Precipitation of Driest Quarter). Maxent 3.4.1 (Phillips et al. 2018) was used to predict the species distribution suitability in combination with presence records and climate layers (Elith et al. 2011). In total, 70% of data were used as training data and 30% were set as test data. Other parameters were left as default, including: maximum 500 iterations, convergence threshold 10⁻⁵, regularization multiplier 1 and 10 replicates with cross-validation method (Phillips et al. 2018). Model accuracy was evaluated by area under the curve (AUC), which ranged between 0.5 (the predicted model is not better than random points) and 1 (the predicted model is very good); AUC > 0.9 is very good and > 0.8 is good (Swets 1988).

To assess the niche differentiation of two species, niche overlap and niche identity tests were examined based on the habitat suitability scores from SDM (Warren et al. 2010). ASCII files were employed by ENMTools 1.3 (Warren et al. 2010) to obtain the percent of niche overlap and niche identity. To validate the percent of niche overlap and niche difference, two criteria were used: Schoener’s D (Warren et al. 2008) and Hellinger’s-based I (Schoener 1968). Schoener’s D calculates the suitable range based on the probability of occupied grid cells. Hellinger’s-based I work similarly to Schoener’s D but without its assumption (Warren et al. 2010). These indices ranged between 0 (complete divergence/no overlap) and 1 (high similarity/complete overlap).

Based on the occurrence records, the distribution range of two species overlapped. Predicted models confirmed the species distribution in southern Iran (Figs 1, 2). AUC values of the models varied from 0.981 ± 0.015 (mean and standard deviation) to 0.893 ± 0.027 for A. khamirensis and A. micropholis, respectively. The model predicted suitable habitat for A. khamirensis in southern coastal regions of Iran from Bushehr province to Sistan-Baluchestan province. The regions included in the prediction near Bandar-e Lengeh reflect the current distribution pattern of the species, but predictions of suitable habitat in Bushehr and Sistan-Baluchestanare outside of the current distribution of the species (Heidari et al. 2013, Šmid et al. 2014) (Fig. 1).

Habitat suitability for A. micropholis was distinctly focused on southeastern Iran, reflecting the current distribution pattern of the species (Heidari et al. 2014, Šmid et al. 2014) (Fig. 2). One of the presence records of A. micropholis was situated outside of the predicted suitable range in Bushehr province (Kamali 2013). This point is far from the western most records of the species in Hormozgan province, suggesting that it could represent a misidentified specimen. The percentage contribution of each bioclimate variables indicated that the greatest contributions to the models were from the minimum temperature of coldest month for A. micropholis and from precipitation seasonality for A. khamirensis (Table 1).

Niche overlap between A. khamirensis and A. micropholis indicated that their niche similarity was lower than 0.5 (Hellinger’s-based I = 0.713 and Schoener’s D = 0.426) supporting the recognition of both taxa at the specific level. The identity test indicated that the null hypothesis regarding niche overlap can be rejected and the two species are distinctly differentiated in their ecological niches. The result of the niche identity test (Fig. 3) showed that predicted niche models for A. khamirensis and A. micropholis were completely separate (D_H0 = 0.725 ± 0.047 vs. D_H1 = 0.420 and I_H0 = 0.920 ± 0.027 vs. I_H1 = 0.710) (Fig. 3).

Figures 1–2. 

Predicted potential distributions of A. khamirensis (1) and A. micropholis (2), generated by MaxEnt. Three main colors show habitat suitability on the map. Warm colors refer to the high suitability level.

Figure 3. 

Results of the identity test. Black arrows refer to the actual niche overlap as calculated by ENMTools (D and I). The bars (with two different patterns) are calculated by replicates with identity test mode.

The notion of evolutionary lineages diverging by occupying different niches is the basis of one of the oldest species concepts (Ecological Species Concept – ESC, Van Valen 1976). Nakazato et al. (2010) suggested – based on SDM analyses of wild tomatoes – that environmentally mediated differentiation, rather than simply geographical isolation, can be the major driving force in species divergence.

Recently, the genus Acanthodactylus was revised and a new species from the A. micropholis complex was described (Heidari et al. 2013). Acanthodactylus khamirensis is distributed in the westernmost part of the range of A. micropholis (Šmid et al. 2014). Although molecular and morphological differentiation of these species was indicated by Heidari et al. (2014), differences in ecological niche occupancy was not reported until the current study.

The habitat suitability prediction for Acanthodactylus micropholis in southeastern Iran showed that its distribution pattern completely covered the predicted area (Fig. 2), but a larger area in southern Iran was predicted for A. khamirensis (Fig. 1). These two species have different ecological requirements, because habitat suitability for A. khamirensis is mostly dependent to the precipitation, but habitat suitability for A. micropholis is primarily dependent on minimum temperature (Table 1). Niche overlap between the two species is low and they are differentiated from each other based on several abiotic factors. Here, this separation has been confirmed and the true calculated niches are far from the hypothesized niches (Fig. 3). The evidence suggests that precipitation seasonality in Hormozgan province can influence the vegetation type of the region, which might provide more suitable conditions for A. khamirensis presence. On the other hand, habitat suitability for A. micropholis is mostly dependent on minimum temperature in winter. This environmental variable may define time of hibernation (Mayhew 1965) and affect the activity period of the species.

The present study indicates ecological niche divergences between the two spiny-toed lacertids of the genus Acanthodactylus and these results corroborate previous molecular and morphological conclusions (Heidari et al. 2014), suggesting that the two species are also valid based on the ESC.

I am pleased to thank from Ann Paterson, who edited the first draft of the manuscript. The manuscript did not undergo grammar revision and any improprieties of English proficiency are the authors’ entire responsibility.