An integrative insight into the diversity, distribution, and biogeography of the freshwater endemic clade of the Ponticola syrman group (Teleostei: Gobiidae) in the Caucasus biodiversity hotspot

Abstract

Freshwater habitats of the Caucasus biodiversity hotspot represent a center of endemism for the gobiid genus Ponticola Iljin, 1927. Hitherto, large‐scale molecular studies, owing to restricted taxon and geographical sampling, have failed to give an elaborate picture of diversity and evolutionary history of these species. Here, to contribute to filling this gap, we assessed taxonomic diversity, phylogeography and evolutionary history for the south Caspian populations of Ponticola presently classified as P. iranicus and P. patimari, using an integrative taxonomic approach comprising an entire geographic range sampling, and analyses of mitochondrial DNA haplotypes, the head lateral line system, otolith shape, and meristic and morphometric variation. All freshwater samples of the P. syrman group belong to a monophyletic clade with two main subclades: a small subclade confined to the upper Sefidroud sub‐basin including the type locality of P. iranicus and a large subclade with three geographically constrained haplogroups (Hg1, Hg2, and Hg3), comprising the rest of the distribution. Hg1 showed an eastern distribution including the type locality of P. patimari, while Hg2 and Hg3 are sister groups with central and western‐central distributions, respectively. The freshwater clade diverged from P. syrman during the Tyurkyanian low stand (~150 m b.s.l. lasting ~0.1 Myr), while the divergence of P. iranicus and P. patimari and radiations within P. patimari took place during the Bakunian high stand (up to 50 m a.s.l. lasting ~378–480 kya). Species delimitation analyses indicated two distinct species, corresponding to each main subclade. Although the otolith shape and lateral line analyses did not reflect with phylogeographic pattern, PCA and DFA plots of meristic and morphometric data showed a clear separation of the two major subclades corresponding to P. iranicus and P. patimari, suggesting the presence of significant morphological variation meriting formal taxonomic recognition. Overall, our findings (i) reveal the presence of two freshwater endemic species in the P. syrman group, and pending further investigation, hypothesize the presence of a third cryptic species; (ii) revise and document a narrow distributional range and low diversity for P. iranicus, in contrast to a wider distributional range and high diversity for P. patimari; (iii) suggest that the climatic oscillations of the Pleistocene were associated with the cladogenesis within the P. syrman group; and (iv) allowed for the recognition of conservation units and proposition of management measures.

Otoliths of Caspian gobies (Teleostei: Gobiidae): Morphological diversity and phylogenetic implications

“…The Ponticola syrman group comprises two freshwater endemic and cryptic species distinguished from each other mainly based on molecular characters and geographic distributions [ 7 ], i.e., P . iranicus endemic to the upper Sefidroud sub-basin, and P .…”

“…patimari endemic to the western freshwater habitats of the south Caspian sub-basin. PCA and DFA plots for the meristic and morphometric data also showed a clear separation of the two species [ 7 ]. Our otolith morphometric variables, inclination angles, and classical shape descriptors show that the otoliths of P .…”

“…patimari are only slightly different in their REx. Also, the otolith shape analysis of 213 specimens representing six sub-basin samples of these species presented a high level of shape variation which did not show congruence with their taxonomy and phylogeographic structure [ 7 ]. Studies suggest that while genetics constrain the overall shape of the otolith itself, environmental conditions may eventually alter the rates of somatic and otolith growth, which in turn may affect otolith shape.…”

“…Fish sampling was approved by the Ethic Committee of Biology Department, Shiraz University (SU-9630190). Taxonomic identifications were accomplished using available keys, primary taxonomic literature, and DNA sequence analysis [ 5 , 7 , 30 , 31 , 33 – 35 , 39 , 41 ]. The skull of each specimen was opened dorsally with a scalpel and the left sagittal otolith was extracted using fine forceps, cleaned in 5% KOH solution (~5 min), washed in distilled water (~5 min), and dried at room temperature.…”

“…On the other hand, detailed discussions of their morphological characters have become rare, and these molecular-based studies suggest phylogenetic relationships that have not been considered with morphological information and therewith inspire new comparative studies to test those relationships. Hitherto, otolith morphology has been studied for just a few species [ 5 – 7 , 38 , 40 , 45 ]. This study, using a taxonomically broad sample, aims to compare the otolith morphology of extant Caspian gobiids at different taxonomic levels based on detailed descriptions and morphometric analysis to reveal the taxonomic and phylogenetic information inscribed in their otoliths.…”