J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 206 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Original Article Morphological Aberrations of the Dirofilariasis, Sindbis Fever and West Nile Fever Vector Culex Theileri (Diptera: Culicidae) in Iran *Shahyad Azari-Hamidian1, 2, Seyed-Mohammad Omrani3 1Research Center of Health and Environment, School of Health, Guilan University of Medical Sciences, Rasht, Iran 2Department of Medical Parasitology, Mycology and Entomology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran 3Department of Medical Parasitology, School of Medicine, Shahrekord University of Medical Sciences, Shahrekord, Iran *Corresponding author: Dr Shahyad Azari-Hamidian, E-mail: azari@gums.ac.ir (Received 28 Jan 2022; accepted 29 June 2022) Abstract Background: Culex theileri (Diptera: Culicidae) is a known vector of pathogens that cause dirofilariasis, Sindbis fever and West Nile fever in Iran. The species is one of the country’s most abundant and widely distributed species. Methods: In order to conduct a faunistic and bionomic study of mosquitoes, larval collection was carried out in Chahar Mahal and Bakhtiari Province of western Iran using dipping method. Results: In total, some 2096 larvae of Cx. theileri were identified. Among the larvae, 1024 (48.9%) displayed aberra- tions and anomalies in the development of cranial seta 1-C (preclypeal seta). Morphological aberrations and anomalies of seta 1-C in the third- and fourth-instar larvae and abdominal terga of the adults of Cx. theileri collected in Iran are discussed and illustrated. Conclusion: More studies are needed throughout the distribution of Cx. theileri to analyze the variation of the species, especially using both morphological and molecular data. Keywords: Anomalous; Abnormal; Character; Morphology; Variation Introduction The genus Culex Linnaeus (Diptera: Cu- licidae) currently includes 779 species compris- ing 26 subgenera (1). The genus consists of at least 34 species of seven subgenera in south- western Asia (2) and 19 species representing five subgenera in Iran (3). The genus compris- es several important vectors of pathogens that cause infections in humans and domesticated animals (3). Culex theileri Theobald belongs to the Theileri Subgroup of the Pipiens Group of Culex (Culex) (2). The species is found in the Afrotropical, Palearctic and Oriental Regions; however, it is mainly a southern Palearctic spe- cies (2). Culex theileri is a known vector of avian Plasmodium in Portugal (4), Turkey (5) and Spain (6); avian Haemoproteus in Spain (6); Dirofilaria immitis (canine heart worm) in Por- tugal (7), Iran (8) and Canary Islands of Spain (9); West Nile virus in South Africa (10) and Iran (11); Sindbis virus in South Africa (10, 12) and Iran (13); Japanese encephalitis virus in China (14); and Rift Valley fever virus in South Africa (15, 16). Additionally, some in- sect-specific flaviviruses (ISFs) were isolated from this species in Myanmar (17), Portugal (18, 19), Spain (18) and Turkey (20) that are designated Culex theileri flavivirus (CxthFV or CTFV). Also, the Wolbachia pipientis en- dosymbiont has been found in Cx. theileri in Portugal (21) and Iran (22). Lewis (23) noted some variation in the num- Copyright © 2022 The Authors. Published by Tehran University of Medical Sciences. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. http://jad.tums.ac.ir/ https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 207 http://jad.tums.ac.ir Published Online: Sep 30, 2022 ber of the branches of setae 5,6-C (inner and median frontal setae) in Cx. theileri larvae in Sudan. Harbach (2) recorded the morphologi- cal variation of the larval and pupal chaetotaxy and gynandromorphism has been reported by Bedford (24) and Sanchez-Murillo et al. (25). Azari-Hamidian et al. (8) showed molecular var- iation of the barcode region of the cytochrome c oxidase I (COI) gene in the species for the first time in Iran. Demirci et al. (26, 27) stud- ied genetic and morphometric variation in Cx. theileri in Turkey. Azari-Hamidian and Har- bach (28) observed one abnormal seta 1-C (preclypeal seta) in a larva of Cx. theileri col- lected in Kurdistan Province of Iran. Culex theileri is widely distributed in Iran, being found in 28 of the 31 provinces of the country (8, 29–32). The species is one of the most abundant species in the country (33, 34). The larvae occur in a wide range of aquatic habitats (29, 33). During a faunal study of mosquitoes in Cha- har Mahal and Bakhtiari Province, Cx. theileri was the most widely distributed and abundant species collected (33, 35). Among the larvae collected, 1024 specimens displayed various ab- errations and anomalies in the cranial chaeto- taxy. Also, variation in the abdominal terga of adults was observed in different areas of Iran. The present paper illustrates these anomalies, aberrations and variations. Materials and Methods The larval collection was carried out in Cha- har Mahal and Bakhtiari Province using dip- ping method. Larvae were temporarily preserved in lactophenol solution and later mounted on mi- croscope slides using Berlese’s medium. Lar- vae and adults were identified using the keys of Azari-Hamidian and Harbach (36). The mor- phological terminology of Harbach and Knight (37, 38), revised and updated in the Mosquito Taxonomic Inventory (1), is used. Photographs were taken by the authors. Voucher specimens were deposited in the Museum of Medical and Veterinary Entomology, School of Health, Gui- lan University of Medical Sciences and the Museum of Medical Entomology, School of Medicine, Shahrekord University of Medical Sciences, Shahrekord. Azari-Hamidian and Har- bach (28) could be consulted for the definitions of aberration, abnormally, anomaly and varia- tion. A brief explanation of the terms, which were used for anomalies and aberrations, is listed in Table 1. Results A total of 2096 larvae of Cx. theileri (25.1 % of all mosquito larvae collected) were iden- tified in collections made in Chahar Mahal and Bakhtiari Province. Among the larvae, 1024 (48.9%) displayed aberrations and anomalies in the development of cranial seta 1-C where- as 1072 (51.1%) had normally spiniform seta 1-C (Fig. 1). Six larvae (0.28%) had one anom- alous additional seta 1-C (Fig. 2) and 1018 (48.57 %) exhibited aberrations in the development of seta 1-C that are listed in Table 2. The most prevalent aberrant feature was bilateral (26.71 %) and unilateral (17.56%) spiculation, recep- tively (Fig. 3). Interesting and rare features ob- served only once in a single larva (0.05%) in- cluded a forked seta 1-C on one side and its mate on the other side with 3 branches (Fig. 6) and a normal spiniform seta 1-C on one side and a filiform seta 1-C on the other side (Fig. 7). Additionally, aberrant scaling of the ab- dominal terga was observed in adults. The ab- dominal terga of Cx. theileri normally have basal pale bands that are produced medially in- to somewhat triangular patches and apical dark scaling is not interrupted by pale scaling (Fig. 9) but in a few specimens, the posterior dark scaling included two patches of pale scales (Fig. 10). http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 208 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Table 1. Brief description of the anomalies and aberrations of seta 1-C in Culex theileri larvae encountered in the pre- sent investigation, Chahar Mahal and Bakhtiari Province, Iran Normal Normal Spiniform, normally developed 1-C without any abnormalities including aberrations (spiculation and branching) and anoma- lies (extra 1-C) (Fig. 1) Abnormal Anomalous (unilaterally double) Extra 1-C on one side (Fig. 2) Aberrant Unilateral or bilateral spiculation One or both sides of 1-C with spiculation at mid-length (Fig. 3) Unilateral or bilateral branching One or both sides of 1-C with a branch at mid-length (Fig. 4) Unilaterally or bilaterally forked One or both sides of 1-C forked apically (Fig. 5) Unilaterally forked on one side and other side with 3 branches 1-C on one side forked; its mate on the other side with 3 branches (Fig. 6) One side spiniform and the other side filiform 1-C on one side spiniform; its mate on the other side filiform (Fig. 7) Abnormal shape Developed differently than the above conditions (Fig. 8) Table 2. Characteristics of seta 1-C observed in Culex theileri larvae collected in Chahar Mahal and Bakhtiari Province, Iran Characteristics n Normal 1072 Abnormal Anomalous (Unilaterally double) 6 Aberrant Unilateral branching 7 Unilaterally forked 23 Unilateral spiculation 368 Unilateral spiculation and unilateral branching 6 Unilateral spiculation, unilateral branching and unilaterally forked 1 Unilateral spiculation and unilaterally forked 8 Bilateral branching 1 Bilateral spiculation 560 Bilateral spiculation and bilateral abnormal shape 1 Bilateral spiculation and bilateral branching 2 Bilateral spiculation and bilaterally forked 2 Bilateral spiculation and unilateral branching 22 Bilateral spiculation, unilateral branching and unilaterally forked 1 Bilateral spiculation, unilateral branching and bilaterally forked 1 Bilateral spiculation and unilaterally forked 13 One of pair spiniform the other filiform 1 One of pair unilaterally forked the other with 3 branches 1 Subtotal 1024 Total 2096 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 209 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Fig. 1. Culex theileri, normal spiniform seta 1-C, Ardal, Chahar Mahal and Bakhtiari Province, Iran (original photo) Fig. 2. Culex theileri, anomalous (extra) seta 1-C on one side (unilaterally double), Esaabad, Chahar Mahal and Bakhtiari Province, Iran (original photo) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 210 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Fig. 3. Culex theileri, aberrant seta 1-C with spiculation at mid-length, Chamnar, Chahar Mahal and Bakhtiari Province, Iran (original photo) Fig. 4. Culex theileri, aberrant seta 1-C with bilateral branching, Sarkhon, Chahar Mahal and Bakhtiari Province, Iran (original photo) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 211 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Fig. 5. Culex theileri, one the pair of seta 1-C forked, Saman, Chahar Mahal and Bakhtiari Province, Iran (original pho- to) Fig. 6. Culex theileri, one seta 1-C forked and the other with 3 branches, Sarkhoon, Chahar Mahal and Bakhtiari Prov- ince, Iran (original photo) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 212 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Fig. 7. Culex theileri, seta 1-C spiniform (normal) on one side and filiform on the opposite side, Razgah, Chahar Mahal and Bakhtiari Province, Iran (original photo) Fig. 8. Culex theileri, seta 1-C with abnormal shape, Alooni, Chahar Mahal and Bakhtiari Province, Iran (original pho- to) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 213 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Fig. 9. Culex theileri, abdominal terga with normal basal pale bands, Kojanagh, Ardebil Province, Iran (original photo) Fig. 10. Culex theileri, abdominal terga with a pair of postmedian patches of pale scales, Astara, Guilan Province, Iran (original photo) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, Sep 2022, 16(3): 206–216 S Azari-Hamidian et al.: Morphological Aberrations of … 214 http://jad.tums.ac.ir Published Online: Sep 30, 2022 Discussion Regarding the variability of Cx. theileri, Har- bach (2) stated: "the larvae and adults, exclud- ing the male genitalia, are extremely variable and exhibit the same degree of variation within local populations that is observed throughout the entire range. Therefore, it appears that only a sin- gle widespread and variable species is involved, yet it is possible that the taxon actually consists of an aggregate of biologically distinct, iso- morphic species". Therefore, it seems that af- ter more than 30 years the situation is the same. For the first time, Azari-Hamidian et al. (8) found a substitution at position 518 (G/A) in the barcode region of the COI gene of Cx. theileri collected in a northwestern province of Iran (Ardebil) which caused one amino acid change (V to M). Later, Demirci et al. (26) studied ge- netic and morphometric variation in Cx. theil- eri in northeastern Turkey and found that alt- hough populations did not display genetic dif- ferentiation, there was a positive correlation be- tween wing (body) size/shape and altitude. Al- so, Demirci et al. (27) observed a single genet- ic polymorphism in Cx. theileri. Conclusion Despite the wide distribution of Cx. theileri and its role in the transmission of pathogens and parasites of diseases in humans and domesticat- ed animals, there is little genetic information about populations in different countries. 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