Next Article in Journal
Coccolithophore Distribution in the Western Black Sea in the Summer of 2016
Previous Article in Journal
Occurrence of Hepatozoon in Some Reptiles from Brazilian Biomes with Molecular and Morphological Characterization of Hepatozoon caimani
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 15
Issue 12
10.3390/d15121193
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Barcoding Mullets (Mugilidae): Genetic Characterization of Exploited Species in Southern Peninsular India

by
Rahul Rajan
1,
Jean-Dominique Durand
2,*,
Liju Thomas
3,
Arya Sidharthan
3,
M. Ashiq Ur Rahman
4,
Bibin Xavier
5 and
Rajeev Raghavan
1
1
Department of Fisheries Resource Management, Kerala University of Fisheries and Ocean Studies (KUFOS), Kochi 682 506, India
2
Marine Biodiversity, Exploitation and Conservation (MARBEC), University of Montpellier-IRD-CNRS, 34095 Montpellier, France
3
Faculty of Ocean Science and Technology, Kerala University of Fisheries and Ocean Studies (KUFOS), Kochi 682 506, India
4
Hajee Karutha Rowther Howdia College, Uthamapalayam 625 533, India
5
Marine Biotechnology, Fish Nutrition and Health Division, Central Marine Fisheries Research Institute (CMFRI), Kochi 682 506, India
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(12), 1193; https://doi.org/10.3390/d15121193
Submission received: 3 November 2023 / Revised: 29 November 2023 / Accepted: 30 November 2023 / Published: 4 December 2023
Browse Figures
Review Reports Versions Notes

Abstract

:
Fishes of the Mugilidae family are poorly known from a taxonomic perspective, largely because of their conservative morphology. In this paper, we aim to fill the knowledge gap and data deficiency regarding the genetic diversity of mullets occurring in southern peninsular India. A comprehensive mitochondrial phylogeny based on 238 COI sequences (78 newly generated) and three species delimitation methods (ASAP, RESL, and ABGD) confirmed the presence of 21 species of mullets within eight genera in southern peninsular India. These include one species each under the genera Rhinomugil Gill 1863, Minimugil Durand, Chen, Shen, Fu, and Borsa, 2012, Plicomugil Schultz 1953, and Ellochelon Whitley 1930; seven species of Planiliza Whitley 1945; four species of Crenimugil Schultz 1946; four species of Osteomugil Luther 1982; and two species of the “Mugil cephalus Linnaeus 1758” complex—though with uncertainty regarding the exact geographic origin of one of the two species of the “Mugil cephalus” complex and one species phylogenetically close to Planiliza subviridis (Valenciennes 1836). We provide an overview of the specific geographical regions in southern peninsular India, and “species groups”, which require future research using an integrative approach, so as to unravel the true extent of mullet diversity and their distribution in the region.

1. Introduction

Mullets, members of the family Mugilidae, are distributed in offshore, coastal, and inland waters along temperate, subtropical, and tropical seas [1], where they are popular in capture fisheries and aquaculture, intricately connected to cultural values [2], and play an influential part in the estuarine and coastal processes [3]. Around 600,000 tons of wild-caught and 266,048 tons of farmed mullets were harvested in 2019 [4], contributing to food security and livelihoods across the tropics.
Though extensively studied since the time of Linnaeus [5], the taxonomy and systematics of Mugilidae have been in a constant state of confusion, with the resolution and delimitation of species (and even generic) boundaries hindered by their conservative morphology and paucity of useful taxonomic characters [6]. For example, only very slight phenotypic variations exist between species within the genera Mugil Linnaeus 1758 and Planiliza Whitley 1945, making delimitation based on traditional morphological characters and meristics challenging, and identification problematic, particularly for non-specialists [7,8]. This has resulted in mullets being underrepresented [9], or erroneously represented, in field guides, checklists, and other compilations. Though the family Mugilidae currently comprises 78 valid species under 26 genera, more than 300 nominal names are known to exist [10].
Many of the advancements in the taxonomy and nomenclature of mullets began after the application of molecular genetic information, which challenged two hundred years of morphology-based taxonomy and indicated that the group comprises a large number of cryptic species [7,11,12,13] and evolutionarily distinct lineages [14]. Considerable levels of genetic divergence have also been observed between (30–5 mya), and within (~10 mya) species, suggestive of long and independent evolutionary histories [15].
India has a long history of utilizing mullets [16,17], with many estuaries and backwaters contributing to both small-scale fisheries [18] and traditional aquaculture. The earliest studies on mullets in India date back to the 19th century with Hamilton’s [19] work in the Ganges, followed by those in southern peninsular India by Cuvier and Valenciennes [20], and Day [21], who recorded 26 species. From the early decades of the 1900s [22], and for the next one hundred years, many studies [23,24,25,26,27,28,29,30,31,32] either entirely (aquaculture, toxicology, biology, life history) or partially (biodiversity checklists, fishery, trade) focused on mullets. Limited taxonomic studies in the 20th century were carried out by John [33], who recorded 15 species from Kayamkulam Lake (Southern India), Sarojini [34], who reviewed the Indian genera of mullets, and Luther [35], who suggested the occurrence of 13 species of mullets in India and subsequently provided new characters for an improved understanding of their taxonomy [36]. Mullet species in India have also been investigated from the perspective of genetic divergence [37], species delimitation [38], and biogeography [39]. Recently, Bhatt and Mankodi [40] provided an annotated checklist on the diversity of mullets from the Indian subcontinent, largely based on secondary literature, accounting for 24 species within 10 genera. The occurrence of species such as Parachelon grandisquamis (Valenciennes 1836) and Planiliza carinata (Valenciennes 1836) in India, which are mentioned in their checklist, is, however, doubtful [41,42], and needs further confirmation.
The mitochondrial cytochrome c oxidase subunit I (COI) gene, utilized in this study, proved its relevance for species boundaries in the Mugilidae family as demonstrated by Durand et al. [9] by comparing the COI variability alone to a dataset involving three different markers. Even though interspecific hybridization cannot be ruled out when using a mitochondrial marker such as the COI gene [43], there have been no previous reports of natural interspecific hybridization in Mugilidae. Furthermore, even if hybridization remains possible, such a process cannot account for the frequency of cases where there is a discrepancy in species identification between morphology and mitochondrial DNA.
In this paper, we aim to determine the genetic diversity of mullets occurring in the marine, coastal, and inland waters of southern peninsular India, a region known for its mullet fisheries, but where only limited research, especially using topotypic specimens, has been conducted on their taxonomy. By characterizing the existing genetic diversity, we aim to identify major species groups and biogeographical regions, which requires comprehensive explorations and taxonomic studies, using an integrative approach [44]. Through this manuscript, we aim to initiate the development of a meticulously curated repository comprising reference DNA barcodes for Indian mullet species. Additionally, we seek to establish a foundational framework that will contribute to shaping the future debate on the taxonomy and systematics of this fish family within the Indian subcontinent.

2. Materials and Methods

Mullet specimens were purchased from fish landing centers, markets, and/or from local fishers operating in the coastal and estuarine regions along the southern Indian peninsula (southwest and southeast coasts) and the Laccadive archipelago. They were primarily identified (as far as possible) using the “Species Identification Sheets” of the Food and Agricultural Organization (FAO) [45] of the United Nations, and González-Castro and Ghasemzadeh [1]. No fish were killed or sacrificed specifically for the purpose of this study, and the sampling protocols were entirely based on dead fish available in markets/landing centers. Therefore, no specific permissions or ethical clearances were required. The fishing locations are represented in Figure 1. Information on the localities where the mullets were captured, was collected from the fishers, and passive georeferencing of sampling locations was achieved through the utilization of fishing-related data, specifically incorporating details such as distance and direction from landing centers (as provided by fishers or vendors).
DNA extraction, PCR amplification (using primer pair FishF1 + FishF2/FishR1; Ward et al. [46]), and sequencing of the mitochondrial COI gene were carried out following Dahanukar et al. [47]. Sequences were aligned using MUSCLE [48], and a maximum likelihood (ML) analysis was performed in IQ-TREE [49], with the best partition scheme and ultrafast bootstrap support for 1000 iterations [50]. Three distinct phylogenetic trees were constructed as follows: (1) A comprehensive phylogenetic tree using a dataset comprising 238 COI sequences representing species of the family Mugilidae, and a 658 bp sequence of Oryzias latipes (Temminck & Schlegel 1846) as an outgroup. This included 78 new sequences generated as part of the current study (archived in BOLD under project MULIN), and 160 published sequences (including mullet COI sequences from the Indian subcontinent, topotypic sequences, and other reference sequences representing Molecular Operational Taxonomic Units (MOTUs) under eight genera concerning the Indian scenario of mullets, as denoted in References [7,9,11,12,39,41]). These sequences were retrieved from the GenBank (www.ncbi.nlm.nih.gov/genbank/ (accessed on 5 June 2023)) [51]. (2) A concise phylogenetic tree (alignment length 501 bp) using representative sequences (comprising a total of 76 sequences, including an outgroup) from each clade as delineated in the comprehensive phylogenetic tree. This tree was developed to provide a brief, yet informative overview of the genetic diversity of Indian mullets. (3) A phylogenetic tree with 78 newly generated sequences along with an outgroup. The newly generated sequences as part of our studies are presented in Table 1, and information about the complete dataset of mullet sequences used to construct the comprehensive phylogenetic tree, including topotypic and reference sequences obtained from GenBank and newly generated sequences, is provided in Supplementary Table S1. In order to avoid misinterpretations of molecular phylogenetic analyses resulting from misidentifications of sequences in genetic databases, the sequences we used, including both topotypic and other reference sequences, were sourced from research that employed a morphological as well as a molecular taxonomic approach (Supplementary Table S2).
The Bayesian information criterion (BIC) was used for COI data to infer phylogenetic relationships. We performed a partition model analysis [52], where one allows each partition to have its own model. The best partition scheme was chosen using ModelFinder [53], in IQ-TREE. Of the seven partition schemes, the best-fit partition model was obtained by optimizing TPM2 + F + I + G4 parameters for partition part1 + part2 + part3. The optimal log-likelihood (ln L) score of the best tree is −6624.878. The ML tree was subsequently used as a basis for species delimitation using the Automatic Barcode Gap Distance (ABGD) [54], using 100,000 Markov chain Monte Carlo (MCMC) generations, a thinning parameter of 100, and a burn-in of 0.1. The output tree was viewed using FigTree v1.4.2. [55].
The accuracy of the Molecular Operational Taxonomic Unit (MOTU) delineations identified using ABGD was evaluated by comparing MOTUs to BINs provided by BOLD [56] obtained from http://www.barcodinglife.org (accessed on 5 June 2023), and based on the RESL algorithm [57] and ASAP (Assemble Species by Automatic Partitioning analysis) [58]. Species delimitation was carried out using the online ABGD version (https://bioinfo.mnhn.fr/abi/public/abgd/abgdweb.html) with default parameters, applying the Kimura K80 (ts/tv 2.0) substitution model, and for ASAP (https://bioinfo.mnhn.fr/abi/public/asap/), we performed the analysis using the Kimura K80 (ts/tv 2.0) substitution model with a recursive split probability of 0.01. Pairwise genetic distances were calculated by employing the Kimura 2-parameter model [59] using MEGA X [60].
Relevant information on type species and type localities follows the Catalog of Fishes [10] and Kottelat [61], and nomenclature follows Durand and Borsa [11]. When a species was identified morphologically, and its DNA barcode matched (>99% of sequence homology) a sequence published and labelled by Durand and Borsa [11], we mentioned the species name by a “cf.” as well as the interim nomenclature proposed by Durand and Borsa [11].

3. Results

The phylogenetic tree (Figure 2; Supplementary Figure S1) represents eight genera of Mugilidae, viz., Crenimugil Schultz 1946, Ellochelon Whitley 1930, Mugil Linnaeus, 1758, Minimugil Durand, Chen, Shen, Fu, and Borsa, 2012, Osteomugil Luther 1982, Planiliza Whitley 1945, Plicomugil Schultz 1953, and Rhinomugil Gill 1863, each of which were confirmed by the presence of topotypic sequences of the type species (marked with # after the sequence accession number in Supplementary Table S1 and information on topotypic and other reference sequences given in Supplementary Table S2). These eight groups include all known mugilid genera occurring in India and close to one-third of all known mugilid genera (26 genera) in the world.
Species delimitation based on the ABGD, RESL, and ASAP analysis confirmed the occurrence of twenty-one Molecular Operational Taxonomic Units (MOTU) of mullets in India. The phylogenetic tree depicting the genetic diversity of Indian mullets is represented in Figure 2. Furthermore, these 21 species are effectively delineated based on the pairwise genetic distance analysis (Figure 3). The phylogenetic tree with newly generated sequences is presented in Figure 4, and a detailed phylogenetic tree showing comprehensive analysis is provided in Supplementary Figure S1. We restrict our results and discussion to the species diversity within southern peninsular India, though our results are largely applicable to the species diversity of the Indian subcontinent and entire Indo-Pacific.
Details on the species diversity within each genus are provided below.
  • Crenimugil Schultz, 1946—Type species: Crenimugil crenilabis (Forsskål 1775) (JQ060435) (“A” in Supplementary Figure S1)
Four species of Crenimugil occur in India including Crenimugil cf. seheli sp. B (Kerala), Crenimugil cf. seheli sp. A (Kerala, Andaman Islands), C. buchanani (eastern coast, including West Bengal and Tamil Nadu), and “Crenimugil sp. C” sensu Durand and Borsa (2015), represented by the sequence JQ045781 from the Vellar Estuary on the southeastern coast.
2.
Plicomugil Schultz, 1953—Type species: Plicomugil labiosus (Valenciennes 1836) (topotype: MN728289) (“G” in Supplementary Figure S1)
The presence of Plicomugil in the Indian subcontinent was identified based on a sequence generated from Agatti Island in the Laccadive archipelago, the Arabian Sea.
3.
Ellochelon Whitley, 1930—Type species: Ellochelon vaigiensis (Quoy & Gaimard 1825) (topotype: JQ060444) (“F” in Supplementary Figure S1)
Our analysis revealed that the species of Ellochelon occurring in the Vellar Estuary is likely to represent an undescribed species, distinct from topotypic E. vaigiensis, or the species “Ellochelon sp. A” sensu Durand and Borsa (2015), based on the results of ABGD, ASAP, and RESL.
4.
Osteomugil Schultz, 1946—Type species: Osteomugil cunnesius (Valenciennes 1836) (topotype: JQ045777) (“E” in Supplementary Figure S1)
Our analysis delineated ten “species groups” within the genus Osteomugil, of which four occur in India. These include (i) “Osteomugil sp. D” sensu Shen and Durand (2016), found in Yanam and the Vellar Estuary on the southeastern coast, and the Thrikkaripur estuary on the southwestern coast; (ii) “Osteomugil sp. C” sensu Shen and Durand (2016), distributed in the coastal and estuarine waters of the eastern coast of India; (iii) O. cunnesius in the Vellar Estuary; and (iv) Osteomugil cf. perusii found in Andhra Pradesh (Kakkinada), Tamil Nadu (Vellar), and throughout the estuarine systems of Kerala.
5.
Planiliza Whitley, 1945—Type species: Planiliza ordensis (Whitley 1945) (topotype: JQ060449–50) (“H” in Supplementary Figure S1)
Of the fourteen species of Planiliza delineated in our analysis (ABGD, RESL, and ASAP), seven are known to occur in India. These include (i) “Planiliza sp. D” sensu Durand and Borsa (2015), one of the most common and abundant species of Planiliza found throughout the estuaries and backwaters of the southwestern state of Kerala; (ii) “Planiliza sp. B” sensu Durand and Borsa (2015), a species recorded first from Malaysia (topotypic sequence KX223926), which is also distributed on the eastern coast of India in the states of West Bengal and Andhra Pradesh; (iii) “Planiliza cf. macrolepis sp. H” phylogenetically identical to “Planiliza sp. H” sensu Durand and Borsa (2015), a species that is often confused in the literature from India (e.g., Sarojini [34]; Kurup [62]; Fischer and Bianchi [63]) and other regions in the Indo-Pacific (e.g., Sri Lanka, the Maldives, the Philippines, and Japan) as being Planiliza macrolepis, but is distinct from Planiliza macrolepis (Smith 1846) sensu stricto (type locality: South Africa; putative topotypes: JQ060425–26; see Durand and Borsa [11]) and is distributed in the estuaries and backwaters of both the southeast (Vellar) and southwest coasts (Cochin, Ashtamudi) of India; (iv) P. klunzingeri, described as being from Mumbai and distributed along the northwestern coast of India (JX983355–57); (v) “Planiliza sp. K” sensu Shen and Durand [39], which occurs in the Bharuch estuary on the northwestern coast (misidentified as Minimugil cascasia in GenBank—JX983495 and JX983496); (vi) “Planiliza cf. subviridis” specimens morphologically identical to P. subviridis but belonging to another MOTU (BIN BOLD:ABY5947), identified in India based on two sequences (JQ045780, JQ045782) from the Vellar Estuary, on the southeastern coast. It is phylogenetically close to P. subviridis and another specimen from Indonesia (JQ060433) identified as Planiliza subviridis but forming a third MOTU (BOLD: ACC0823); and (vii) P. subviridis, a species described as coming from the erstwhile British Indian region of Malabar (current day northern Kerala State/Southern Karnataka State) represented by topotypic sequences (MG495936, MN728289, MN728299, MN728294, MN728292, MN728296) and several additional matching sequences confirming their wide distribution throughout the coastal and estuarine waters of the entire eastern (West Bengal, Andhra Pradesh, and Tamil Nadu), as well as southwestern coasts (Kerala).
6.
Mugil Linnaeus, 1758—Type species: Mugil cephalus Linnaeus 1758 (topotypes: KY683176, JQ060529, JQ060532–34) (“C” in Supplementary Figure S1)
The species delimitation analysis using ABGD, ASAP, and RESL delineated the Mugil cephalus clade into five “species groups” or lineages. Two species groups within the “Mugil cephalus complex” are likely to occur in India. The first species (“species group” number “3” in Supplementary Figure S1) did not match any lineages highlighted by Durand et al. [7] or Durand and Borsa [11]. It comprised sequences originating from both the southeastern and southwestern coasts of India. Outside India this MOTU (BOLD: ADZ0803) has been observed in Bangladesh, Pakistan, and Iran (BOLD, consultation on 02/08/2023). It is phylogenetically close to the species provisionally named as “Mugil sp. L” by Durand and Borsa [11], and observed in the Pacific from Taiwan to New Caledonia and Fiji [64].
A likely second species group within the “Mugil cephalus complex” could occur in India based on three sequences (KT347596–98) from the Vellar Estuary, on the southeastern coast. This species has been identified as “Mugil sp. I” by Durand and Borsa [11]. With the exception of the three specimens from the Vellar Estuary, it is only observed in the Northwest Pacific from Japan to Vietnam and the Philippines [64].
7.
Rhinomugil Gill, 1863—Type species: Rhinomugil corsula (topotype: JX105471) (“A” in Supplementary Figure S1)
Only one species, Rhinomugil corsula, occurs in the Indian subcontinent, confirmed through a topotypic sequence available in GenBank (JX105471). The distribution range of this species includes the estuarine and riverine systems on the eastern and western coasts of India with confirmed genetic data from the states of Assam, West Bengal, Andhra Pradesh, and Gujarat.
8.
Minimugil Durand, Chen, Shen, Fu, and Borsa, 2012—Type species: Minimugil cascasia (Hamilton 1822) (topotypes: JQ060624 and MK572330) (“B” in Supplementary Figure S1)
No sequence of this species was generated as part of this study, and, also, no sequences are available in GenBank from the Indian region that match putative topotypic sequences from Bangladesh (JQ060624 and MK572330). Given the geographic proximity of Bangladesh to the northeastern coast of India (West Bengal), it is highly likely that this species is distributed in the estuaries of India, but this needs to be confirmed by future studies.

4. Discussion

Mullets are major contributors to brackish-water and estuarine fisheries along both the western and eastern coasts of India [35], and are also emerging candidates for brackish-water aquaculture diversification [65,66]. This has made species identification a priority, so as to inform conservation, management, trade, and policy. To the best of our knowledge, there have been no previous studies from the Indian subcontinent, where mullet species have been delineated and identified using topotypic material and/or sequences—a knowledge gap we address in our study.
The taxonomy and nomenclature of mullets is in flux, and recent research, particularly using molecular genetic information, has challenged two hundred years of morphology-based taxonomy (e.g., [7,11]). This is because previous studies on Indian species of mullets were mainly based on conventional taxonomy, and identification was mainly based on the personal perceptions of authors. Since the 1950s, most authors who working on mullet taxonomy have (i) provided conflicting opinions and statements regarding the morphology and meristics of the various “species” recorded from India (See Supplementary Table S3), (ii) used diagnostic characters that have subsequently been proved as unreliable for identification (e.g., those that change during ontogenic development—adipose eyelids, types of scales, mandibular angle, third anal fin spine) [22,67], and (iii) erroneously assigned species to various genera [18,22,35,68,69,70,71], without proper justification.
Most historic records (1800s to the early 20th century) of mullets in the Indian literature have assigned the species to either of the two genera, i.e., Mugil or Liza [21,22,33,67,68]. Generic-level revisions carried out since then have significantly changed our understanding of mullet taxonomy and nomenclature, but the absence of systematic genetic studies on mullets in India makes the comparison of our results difficult.
Our analysis reveals that three monotypic genera, Rhinomugil (R. corsula), Plicomugil (P. labiosus) and Minimugil (M. cascasia) occur in India. Of these, the occurrence of Plicomugil was confirmed based on a topotypic sequence from the Laccadive archipelago and Rhinomugil from a topotypic sequence from Assam. Previous records on Plicomugil labiosus are available from Lakshadweep waters [72]. The likely occurrence of Minimugil in Indian waters is suggested based on sequences collected from neighboring Bangladesh (as no sequences are as yet available from India), as this location is also part of the Indian subcontinent. Ellochelon, which has been considered monotypic [10], is also likely to contain additional species, as evident from our species delimitation, and as suggested by Durand and Borsa 2016 [11], and more recent studies [73,74].
Apart from Crenimugil cf. seheli sp. A (in Kerala) and C. buchanani (eastern coast including West Bengal and Tamil Nadu), two other species of the genus occur in Indian waters. One species, which we identify as Crenimugil cf. seheli sp. B, distributed along the southwestern coast and in the Andaman and Nicobar Islands, may be considered to be a distinct species named as Crenimugil sp. B sensu Durand & Borsa [11] since two species delimitation methods separate Indian specimens from other specimens named Crenimugil sp. B. However, this result needs to be strengthened using a larger dataset able to improve inter- and intraspecies diversity estimation, and thus the barcode gap detection. The second unnamed species, which we consider as “Crenimugil sp. C”, occurs in the Vellar Estuary on the southeastern coast of India.
The Osteomugil clade (clade E in Supplementary Figure S1) comprises Osteomugil cunnesius, Osteomugil cf. perusii, and two other species, which we list as “Osteomugil sp. D” (southeastern and southwestern coasts) and “Osteomugil sp. C”, (eastern coast). Osteomugil cunnesius is confirmed based on the topotypic sequence (JQ045777) from the Vellar Estuary. Osteomugil perusii is associated with four BINs (Supplementary Table S1), but only three MOTUs are considered following species delimitation analyses (ABGD, RESL, and ASAP). In India, the two BINs (AEZ8463 and AAW7354) converge into a single MOTU. The geographic distribution of the three BINs linked to the three MOTUs is as follows: BIN BOLD: ACC0135 is observed in New Caledonia, Papua New Guinea, and Indonesia; BIN BOLD: AAW7354 is found in Indonesia, India, the Philippines, Malaysia, and Sri Lanka; and BIN BOLD: ACC0061 is present in Malaysia, Indonesia, China, and Taiwan. These three BINs exhibit some overlap in Indonesia, as mentioned in Delrieu-Trottin [8], although this overlap appears to be partial. This leads to the suggestion that BIN BOLD: ACC0135 represents Osteomugil perusii sensu stricto, given the species’ type locality is in Vanikoro Island and Santa Cruz Islands in the southwestern Pacific. The remaining two BINs may be considered sister species, with one primarily inhabiting the Indian Ocean (species group number “10” in Figure 2) and the other in the NW Pacific. The identity of the species found in India may be considered as Mugil amarulus Valenciennes, 1836, a synonym of Osteomugil perusii [10], but requires further studies for confirmation. To assign a species name to Osteomugil sp. C and Osteomugil sp. D, more detailed morphological investigations are needed.
Planiliza is probably the most species-rich mullet genus in the Indo-Pacific, represented by at least fourteen “species groups” (clade H in Supplementary Figure S1), of which seven are known to occur in India. The species found in India, identified and validated by matching topotypic sequences, include P. klunzingeri and P. subviridis. The second putative species closely related to Planiliza subviridis and “Planiliza cf. subviridis [BOLD: ACC0823]” (JQ060433 from Indonesia) designated as “Planiliza cf. subviridis” in Table 1 and assigned to the BIN BOLD: ABY5947 occurs in the Vellar Estuary, on the southeastern coast of India. This BIN ABY5947 includes specimens from eastern Asia including from China and Taiwan. The presence of this species in the natural waters of India is also doubtful similar to the occurrence of “Mugil sp. I”, and could probably correspond to fish imports [75]. To confirm the identity of four additional species occurring in Indian waters (Planiliza sp. B, D, H, and K), detailed taxonomic studies are required. Two of these species have a distribution primarily on the west coast of India: “Planiliza sp. D” (Cochin backwaters to the Bharuch estuary in Gujarat) and “Planiliza sp. K” (Bharuch estuary in Gujarat). Planiliza sp. H is closely allied to P. macrolepis—a species described as coming from the rivers and lakes of South Africa [76], and currently known throughout the Indo-West Pacific. The clade comprising the sequences JQ060425–26 originating from South Africa and the Seychelles is considered topotypic for the present analysis, and is distinct from the specimens misidentified as P. macrolepis in India—which we designated as “Planiliza cf. macrolepis sp. H” since no significant divergence was observed between specimens from Sri Lanka and the Maldives named by Durand and Borsa [11] as Planiliza sp. H. It can be noticed in Figure 2 (also in Supplementary Figure S1) that specimens named by Durand and Borsa [11] as Planiliza sp. H form two distinct MOTUs irrespective of the species delimitation method used (BINs BOLD: ACC0087 and BOLD:AAC0697). However, Durand and Borsa [11] did not acknowledge this genetic differentiation despite evident geographic disconnection in the BIN’s geographic distribution since genetic divergence evaluated using three mitochondrial markers is not significant (see Figure 1 in Durand and Borsa [11]). Three of these putative species (Planiliza sp. K, H, and D) occur in the estuarine waters of the west coast (two also on the east coast) where several names, which are now considered synonyms of P. macrolepis, are available. For example, Mugil cunnumboo Day, 1865 (type locality: Malabar, India), and Mugil olivaceus Day, 1876 (type locality: Seas of India ascending rivers), could be assigned to “Planiliza cf. macrolepis sp. H” pending detailed taxonomic studies, and the conspecificity of Planiliza mandapamensis (Thomson, 1997) can be determined with specimens of either “Planiliza sp. K” and “Planiliza sp. D”.
The cosmopolitan Mugil cephalus, which has been shown to be a species complex [14,64,77,78], is one of the most commonly listed mullet species in the Indian literature, recorded from both coasts of the region. Though the Mugil cephalus clade (clade C in Supplementary Figure S1) was well-resolved in the mitochondrial COI phylogeny, and the subsequent ABGD, RESL, and ASAP analysis delineated at least five groups despite limited sampling of this species complex (in Supplementary Figure S1). We consider these as “putative species”, with two of them represented in Indian waters. The first putative species has a distribution on the eastern and western coasts of India where a name, Mugil cephalotus Valenciennes, 1836 (type locality: Malabar and Pondicherry, India), is already available. Mugil cephalotus is currently considered to be a synonym of M. cephalus, and has been described as coming from erstwhile provinces of Malabar (west coast/Arabian sea) and Pondicherry (east coast/Bay of Bengal) in southern peninsular India [20]. The presence of a genetically distinct species within the genus Mugil from both the southwestern and southeastern coasts of India necessitates the need for a separate name. The name M. cephalotus can be tentatively used to represent this genetically distinct lineage, as it is the oldest available name for a species aligned to M. cephalus from southern India. The revalidation of this name should, however, be carried out after detailed morphological examination using topotypic specimens and available syntypes, representative of a larger geographic sampling to determine the exact distribution range of this species.
The sequence FJ384686, identified as Mugil cephalus in GenBank, is also part of this group, but the location provided (11.48° N and 76.76° E) points to the Nilgiri hills in the Western Ghats Mountain range, at an altitude of >2000 m above sea level. It is highly unlikely that a species of the Mugil cephalus complex occurs at such a high altitude, and the location and coordinates provided by the authors could therefore be erroneous. The second putative species in the Mugil cephalus complex occurs in the Vellar Estuary, on the southeastern coast of India. This lineage, which was designated as “Mugil sp. I” in Durand and Borsa [11], includes specimens from eastern Asia (e.g., Vietnam, China, Taiwan, and Japan). This fish (i.e., “Mugil sp. I”) has also been observed in the markets of Bangladesh (E. Hasan, pers. comm.). The presence of this species in the natural waters of India is doubtful, and could likely correspond to fish imports from countries such as China [76] where “Mugil sp. I” (or Northwest Pacific 2 sensu Shen et al., 2011) is largely reared in aquaculture for the production of bottarga (a local delicacy made from the roe) [79].
Although mullets have been recorded in checklists and other compilations from major estuaries on the eastern and western coasts of India, the available sequences in GenBank mainly originate from three major areas: the Vellar Estuary in Tamil Nadu (18 sequences), the Bharuch estuary in Gujarat (8 sequences), and the Cochin Backwaters (10 sequences). Despite adding 78 new sequences from the coastal and estuarine waters of the southwestern coast of India as part of this study, there remain many geographical areas that are known for their mullet diversity (e.g., Chilika Lake in Odisha, Pulicat Lake and Mandapam backwaters in Tamil Nadu, and the Zuari and Mandovi estuaries in Goa) where intensive surveys complemented by barcoding will be required in the future. This is in addition to the need for integrative taxonomic studies (morphology, anatomy, and genetics) for genera such as Planiliza, Osteomugil, and the Mugil cephalus species complex, to identify their true diversity and fine-scale distribution.

5. Conclusions

Our results, based on a comprehensive mitochondrial phylogeny and species delimitation of 238 COI sequences, confirmed the presence of 21 species of mullets within eight genera in India. This includes one species each under the genera Rhinomugil, Minimugil, Plicomugil, and Ellochelon; seven species of Planiliza; four species of Crenimugil; four species of Osteomugil; and two species of the Mugil cephalus complex. Overall, the results of our study will help improve the knowledge of the diversity and distribution of one of the most important groups of brackish-water and coastal finfish species of the Indian subcontinent.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d15121193/s1, Supplementary Figure S1: Maximum likelihood phylogenetic tree of family Mugilidae from the Indo-Pacific and their species delimitation using ABGD, ASAP, and RESL; Supplementary Table S1: Details of species, locations, GenBank accession numbers, and BIN ID (BOLD) for the mullet sequences included in the phylogenetic tree presented in Supplementary Figure S1; Supplementary Table S2: Details of topotypic and other reference sequences obtained from GenBank; Supplementary Table S3: Discrepancies observed in morphological characters used in previous studies on Indian mullets. Refs. [80,81,82,83,84,85] are cited in SM file.

Author Contributions

R.R. (Rahul Rajan) and R.R. (Rajeev Raghavan) conceived the study. R.R. (Rahul Rajan), B.X. and M.A.U.R. undertook field surveys, carried out morphological examinations, and contributed to laboratory work. J.-D.D., L.T. and A.S. carried out the laboratory work. J.-D.D., A.S., R.R. (Rajeev Raghavan), R.R. (Rahul Rajan) and B.X. performed the phylogenetic analysis. M.A.U.R. and J.-D.D. contributed sequences and other resources. R.R. (Rahul Rajan), J.-D.D. and R.R. (Rajeev Raghavan) co-wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

R. Rajan thanks the Head of the Department of Fisheries Resource Management and the Dean of the Fisheries Faculty, Kerala University of Fisheries and Ocean Studies (KUFOS), for the facilities and funding provided. R. Raghavan thanks the Center for Aquatic Resource Management and Conservation (CARMAC), KUFOS, for their funding. IRD funded the DNA barcoding for half of the specimens analyzed in this study.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All sequences generated as part of the study and used in the analysis are deposited in GenBank and BOLD (details and accession numbers provided in the table and figures).

Acknowledgments

The authors thank Anvar Ali for their useful discussions; Neelesh Dahanukar for his help with the phylogenetic analysis; M. Mubarak, V.K Anoop, Albin Albert C., Rose P. Bright, P.K. Athira, and K.C. Adarsh for their help and support during the fieldwork, and in the preparation of the manuscript; and K. Ranjeet, Department of Aquatic Environment Management, for the laboratory facilities.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. González-Castro, M.; Ghasemzadeh, J. Morphology and morphometry-based taxonomy of Mugilidae. In Biology, Ecology and Culture of Grey Mullets (Mugilidae); Crosetti, D., Blaber, S., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 1–20. [Google Scholar] [CrossRef]
  2. Crosetti, D. Current state of grey mullet fisheries and culture. In Biology, Ecology and Culture of Grey Mullets (Mugilidae); Crosetti, D., Blaber, S., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 398–450. [Google Scholar] [CrossRef]
  3. Lefeuvre, J.C.; Laffaille, P.; Feunteun, E. Do fish communities function as biotic vectors of organic matter between salt marshes and marine coastal waters? Aquat. Ecol. 1999, 33, 293–299. [Google Scholar] [CrossRef]
  4. FAO Yearbook. Fish. Aquacult. Stat. 2019/FAO Annuaire. Statistiques des Pêches et de L’aquaculture 2019/FAO Anuario. Estadísticas de Pesca y Acuicultura 2019; FAO: Rome, Italy, 2021; 82p. [Google Scholar]
  5. Linnaeus, C.V. Systems Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Editio Decima, Reformata. Laurentii Salvii: Stockholm, Sweden, 1758; Volume 1, 824p. [Google Scholar]
  6. Harrison, I.J.; Nirchio, M.; Oliveira, C.; Ron, E.; Gaviria, J. A new species of mullet (Teleostei: Mugilidae) from Venezuela, with a discussion on the taxonomy of Mugil gaimardianus. J. Fish Biol. 2007, 71, 76–97. [Google Scholar] [CrossRef]
  7. Durand, J.D.; Shen, K.N.; Chen, W.J.; Jamandre, B.W.; Blel, H.; Diop, K.; Nirchio, M.; Garcia de León, F.J.; Whitfield, A.K.; Chang, C.W.; et al. Systematics of the grey mullets (Teleostei: Mugiliformes: Mugilidae): Molecular phylogenetic evidence challenges two centuries of morphology-based taxonomy. Mol. Phylogenet. Evol. 2012, 64, 73–92. [Google Scholar] [CrossRef] [PubMed]
  8. Delrieu-Trottin, E.; Durand, J.D.; Limmon, G.; Sukmono, T.; Kadarusman; Sugeha, H.Y.; Chen, W.J.; Busson, F.; Borsa, P.; Dahruddin, H.; et al. Biodiversity inventory of the grey mullets (Actinopterygii: Mugilidae) of the Indo-Australian Archipelago through the iterative use of DNA-based species delimitation and specimen assignment methods. Evol. Appl. 2020, 13, 1451–1467. [Google Scholar] [CrossRef] [PubMed]
  9. Durand, J.D.; Hubert, N.; Shen, K.N.; Borsa, P. DNA barcoding grey mullets. Rev. Fish Biol. Fish. 2017, 27, 233–243. [Google Scholar] [CrossRef]
  10. Fricke, R.; Eschmeyer, W.N.; van der Laan, R. Eschmeyer’s Catalog of Fishes: Genera, Species, References. 2023. Available online: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (accessed on 24 January 2023).
  11. Durand, J.D.; Borsa, P. Mitochondrial phylogeny of grey mullets (Acanthopterygii: Mugilidae) suggests high pro-portion of cryptic species. CR Biol. 2015, 338, 266–277. [Google Scholar] [CrossRef]
  12. Durand, J.D. Implications of molecular phylogeny for the taxonomy of Mugilidae. In Biology, Ecology and Culture of Grey Mullets (Mugilidae); Crosetti, D., Blaber, S., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 22–41. [Google Scholar] [CrossRef]
  13. Xia, R.; Durand, J.D.; Fu, C. Multilocus resolution of Mugilidae phylogeny (Teleostei: Mugiliformes): Implications for the family’s taxonomy. Mol. Phylogenet. Evol. 2016, 96, 161–177. [Google Scholar] [CrossRef]
  14. Bae, E.B.; Kim, J.K.; Li, C. A new perspective on biogeographic barrier in the flathead grey mullet (Pisces: Mugilidae) from the northwest Pacific. Genes Genom. 2020, 42, 791–803. [Google Scholar] [CrossRef]
  15. Neves, J.M.M.; Almeida, J.P.F.A.; Sturaro, M.J.; Fabré, N.N.; Pereira, R.J.; Mott, T. Deep genetic divergence and paraphyly in cryptic species of Mugil fishes (Actinopterygii: Mugilidae). Syst. Biodivers. 2020, 18, 116–128. [Google Scholar] [CrossRef]
  16. Pillay, T.V.R. On the culture of grey mullets in association with commercial carps in freshwater tanks in Bengal. J. Bombay Nat. Hist. Soc. 1949, 48, 601–604. [Google Scholar]
  17. FAO. Mugil cephalus; Cultured Aquatic Species Information Programme; FAO: Rome, Italy, 2006–2021; Available online: https://www.fao.org/fishery/en/culturedspecies/Mugil_cephalus/en (accessed on 14 October 2022).
  18. Panda, D.; Mohanty, S.K.; Pattnaik, A.K.; Das, S.; Karna, S.K. Growth, mortality and stock status of mullets (Mugilidae) in Chilika Lake, India. Lakes Reserv. Sci. Policy Manag. Sustain. Use 2018, 23, 4–16. [Google Scholar] [CrossRef]
  19. Hamilton, F. An Account of the Fishes Found in the River Ganges and Its Branches; Archibald Constable and Company: Edinburgh, UK; London, UK, 1822; 405p. [Google Scholar] [CrossRef]
  20. Cuvier, G.; Valenciennes, A. Histoire Naturelle des Poisons; Chez, F.G., Ed.; Levrault: Paris, France, 1836; Volume 11, 506p. [Google Scholar]
  21. Day, F. The Fishes of India; Being a Natural History of the Fishes Known to Inhabit the Seas and Fresh Waters of India Burma, and Ceylon; Bernard Quaritch: London, UK, 1878; Volume 1, 778p. [Google Scholar] [CrossRef]
  22. Whitehouse, R.H. The grey mullets of Tuticorin. Madras Fish Bull. 1922, 15, 71–98. [Google Scholar]
  23. Kutty, M.N.; Sukumaran, N.; Kasim, H.M. Influence of temperature and salinity on survival of the freshwater mullet, Rhinomugil corsula (Hamilton). Aquaculture 1980, 20, 261–274. [Google Scholar] [CrossRef]
  24. James, P.S.B.R.; Rengaswamy, V.S.; Raju, A.; Mohanraj, G. Studies on diurnal variations in the occurrence of grey mullet seed at Mandapam. In Proceedings of the Symposium on Coastal Aquaculture, Marine Biological Association of India; Silas, E.G., Rao, P.V., Nakayana Rao, K.V., George, K.C., Rengarajan, K., Pillai, P.P., Krishnan, L., Eds.; The Diocesan Press: Madras, India, 1984; pp. 765–775. [Google Scholar]
  25. Rekharani, Z.; Madhavi, R. Digenetic trematodes from mullets of Visakhapatnam (India). J. Nat. Hist. 1985, 19, 929–951. [Google Scholar] [CrossRef]
  26. Lazarus, S.; Nandakumaran, K. The intensive farming of striped Mullet, Mugil cephalus (Linnaeus 1758), in the polyethylene film-lined ponds developed on the sea shore at Calicut, Kerala. In Aquaculture Productivity; Sinha, V.R.P., Srivastava, H.C., Eds.; OXFORD and IBH Publishing CO. PVT. LTD: New Delhi, India, 1991; pp. 521–531. [Google Scholar]
  27. George, K.C.; Pandey, A.K.; Peer Mohamed, M. Mercury chloride induced renal lesions in the mullet Liza parsia (Hamilton-Buchanan). J. Mar. Biol. Assoc. India 1995, 37, 179–184. [Google Scholar]
  28. Nayak, J.; Viswanathan Nair, P.G.; Ammu, K.; Mathew, S. Lipase activity in different tissues of four species of fish: Rohu (Labeo rohita Hamilton), oil sardine (Sardinella longiceps Linnaeus), mullet (Liza subviridis Valenciennes) and Indian mackerel (Rastrelliger kanagurta Cuvier). J. Sci. Food Agric. 2003, 83, 1139–1142. [Google Scholar] [CrossRef]
  29. Laxmi Priya, S.; Senthilkumar, B.; Hariharan, G.; Paneer Selvam, A.; Purvaja, R.; Ramesh, R. Bioaccumulation of heavy metals in mullet (Mugil cephalus) and oyster (Crassostrea madrasensis) from Pulicat lake, south east coast of India. Toxicol. Ind. Health 2011, 27, 117–126. [Google Scholar] [CrossRef] [PubMed]
  30. Hariharan, G.; Purvaja, R.; Ramesh, R. Environmental safety level of lead (Pb) pertaining to toxic effects on grey mullet (Mugil cephalus) and Tiger perch (Terapon jarbua). Environ. Toxicol. 2014, 31, 24–43. [Google Scholar] [CrossRef]
  31. Ghosh, S.; Ranjan, R.; Megarajan, S.; Pattnaik, P.; Dash, B.; Edward, L. Mixed culture of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) and flathead grey mullet Mugil cephalus (Linnaeus, 1758) in floating cages. Indian J. Fish. 2016, 61, 63–69. [Google Scholar] [CrossRef]
  32. Swain, S.; Chadha, N.K.; Sundaray, J.K.; Sawant, P.B.; Chhandaprajnadarsini, E.M. Effect of vitamin C dietary supplementation on growth and survival of grey mullet, Mugil cephalus (Linnaeus, 1758) fry. Asian J. Microbiol. Bio Technol. Environ. Sci. 2016, 18, 645–649. [Google Scholar]
  33. John, C.M. The grey mullets of Kayamkulam Lake, India and their fishery. Copeia 1955, 1955, 225–230. [Google Scholar] [CrossRef]
  34. Sarojini, R.P. A revision of Indian Mugilidae. Part I and II. J. Bombay Nat. Hist. Soc. 1962, 59, 254–270. [Google Scholar]
  35. Luther, G. The grey mullet fishery resources of India. In Proceedings of the Symposium on Living Resources of the Seas around India; Special Publication. Central Marine Fisheries Research Institute: Cochin, India, 1973; pp. 455–460. [Google Scholar]
  36. Luther, G. New characters for consideration in the taxonomic appraisal of grey mullets. J. Mar. Biol. Assoc. India 1977, 19, 1–9. [Google Scholar] [CrossRef]
  37. Menzes, M.R.; Martins, M.; Naik, S. Interspecific genetic divergence in grey mullets from the Goa region. Aquaculture 1992, 105, 117–129. [Google Scholar] [CrossRef]
  38. Rahman, A.U.; Khan, S.A.; Lyla, P.; Kumar, C.P. DNA barcoding resolves taxonomic ambiguity in mugilidae of Parangipettai waters (southeast coast of India). Turk. J. Fish. Aquat. Sci. 2013, 13, 321–330. [Google Scholar] [CrossRef]
  39. Shen, K.N.; Durand, J.D. The biogeography of Mugilidae in India South-East and East Asia. In Biology, Ecology and Culture of Grey Mullets (Mugilidae); Crosetti, D., Blaber, S., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 63–84. [Google Scholar]
  40. Bhatt, D.M.; Mankodi, P.C. An annotated checklist of family Mugilidae Jarocki, 1822 (Actinopterygii: Mugiliformes) from India. J. Asia Pac. Biodivers. 2022, 16, 5–19. [Google Scholar] [CrossRef]
  41. Durand, J.D.; Whitfield, A.K. Biogeography and distribution of Mugilidae in the western, central and southern regions of Africa. In Biology, Ecology and Culture of Grey Mullets (Mugilidae); Crosetti, D., Blaber, S., Eds.; CRC Press: Boca Raton, FL, USA, 2016; pp. 102–115. [Google Scholar]
  42. Hasan, M.E.; Hasan, A.; Béarez, P.; Shen, K.N.; Chang, C.W.; Tran, T.T.V.; Golani, D.; Al-Saboonchi, A.; Siddiqui, P.J.A.; Durand, J.D. Planiliza lauvergnii (Eydoux and Souleyet, 1850), a senior synonym of Planiliza affinis (Günther, 1861) with a re-evaluation of keeled back mullets (Mugiliformes: Mugilidae). Zootaxa 2022, 5194, 497–518. [Google Scholar] [CrossRef]
  43. Ward, R.D. DNA barcode divergence among species and genera of birds and fishes. Mol. Ecol. Resour. 2009, 9, 1077–1085. [Google Scholar] [CrossRef]
  44. Padial, J.M.; Miralles, A.; De la Riva, I.; Vences, M. The integrative future of taxonomy. Front. Zool. 2010, 7, 16. [Google Scholar] [CrossRef]
  45. Harrison, I.J.; Senou, H. Mugilidae. Bony Fishes Part 2 (Mugilidae to Carangidae). In FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific; Carpenter, K.E., Niem, V.H., Eds.; FAO: Rome, Italy, 1999; Volume 4, pp. 2069–2108. [Google Scholar]
  46. Ward, R.D.; Zemlak, T.S.; Innes, B.H.; Last, P.R.; Hebert, P.D.N. DNA barcoding Australia’s fish species. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360, 1847–1857. [Google Scholar] [CrossRef]
  47. Dahanukar, N.; Philip, S.; Krishnakumar, K.; Ali, A.; Raghavan, R. The phylogenetic position of Lepidopygopsis typus (Teleostei: Cyprinidae), a monotypic freshwater fish endemic to the Western Ghats of India. Zootaxa 2013, 3700, 113–139. [Google Scholar] [CrossRef] [PubMed]
  48. Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [PubMed]
  49. Nguyen, L.T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef] [PubMed]
  50. Hoang, D.T.; Chernomor, O.; Haeseler, A.V.; Minh, B.Q.; Vinh, L.S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 2018, 35, 518–522. [Google Scholar] [CrossRef] [PubMed]
  51. Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2016, 44, 67–72. [Google Scholar] [CrossRef] [PubMed]
  52. Chernomor, O.; Von Haeseler, A.; Minh, B.Q. Terrace aware data structure for phylogenomic inference from super matrices. Syst. Biol. 2016, 65, 997–1008. [Google Scholar] [CrossRef] [PubMed]
  53. Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; Haeseler, A.V.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef] [PubMed]
  54. Pullandre, N.; Lambert, A.; Brouillet, S.; Achaz, G. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol. Ecol. 2012, 21, 1864–1877. [Google Scholar] [CrossRef]
  55. Rambaut, A. FigTree; Version 1.4.2; Inst. Evol. Biol.; University of Edinburgh: Edinburgh, UK, 2014; Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 5 June 2023).
  56. Ratnasingham, S.; Hebert, P.D. BOLD: The Barcode of Life Data System. Mol. Ecol. Notes 2007, 7, 355–364. [Google Scholar] [CrossRef]
  57. Ratnasingham, S.; Hebert, P.D.N. A DNA-based registry for all animal species: The barcode index number (BIN) system. PLoS ONE 2013, 8, e66213. [Google Scholar] [CrossRef]
  58. Puillandre, N.; Brouillet, S.; Achaz, G. ASAP: Assemble species by automatic partitioning. Mol. Ecol. Resour. 2020, 21, 609–620. [Google Scholar] [CrossRef] [PubMed]
  59. Kimura, M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16, 111–120. [Google Scholar] [CrossRef] [PubMed]
  60. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
  61. Kottelat, M. The fishes of the inland waters of Southeast Asia: A catalogue and core bibliography of the fishes known to occur in freshwaters, mangroves and estuaries. Raffles Bull. Zool. 2013, 27, 1–663. [Google Scholar]
  62. Kurup, B.M. Studies on the Systematics and Biology of the Fisheries of the Vembanad Lake. Ph.D. Thesis, Cochin University of Science and Technology, Kochi, India, 1982; 683p. [Google Scholar]
  63. Fischer, W.; Bianchi, G. Species Identification Sheets for Fishery Purposes; Western Indian Ocean (Fishing Area 51); FAO: Rome, Italy, 1984; Volume III. [Google Scholar]
  64. Tran, T.T.V.; Ke Phan, L.; Durand, J.D. Diversity and distribution of cryptic species within the Mugil cephalus species complex in Vietnam. Mitochondrial DNA Part A 2016, 28, 493–501. [Google Scholar] [CrossRef] [PubMed]
  65. Syama Dayal, J.; Ambasankar, K.; Jannathulla, R.; Kumaraguruvasagam, K.P.; Kailasam, M.; Vijayan, K.K. Poly-culture of mullets in brackishwater using compounded feed: Proximate and mineral profiles in comparision with wild mullets. Indian J. Fish. 2017, 64, 50–57. [Google Scholar] [CrossRef]
  66. Sukumaran, K.; Thomas, D.; Rekha, M.U.; Angel, J.R.J.; Bera, A.; Mandal, B.; Subburaj, R.; Thiagarajan, G.; Makesh, M.; Ambasankar, K.; et al. Reproductive maturation and induced breeding of two geographical groups of grey mullet, Mugil cephalus Linnaeus, 1758. Aquaculture 2021, 536, 736423. [Google Scholar] [CrossRef]
  67. Day, F. The Fishes of Malabar; Bernard Quaritch: London, UK, 1865; 293p. [Google Scholar]
  68. Chaudhuri, B.L. Fauna of the Chilka Lake Fish Part III. Mem. Indian Mus. 1917, 5, 491–508. [Google Scholar]
  69. Shekhar, M.S.; Natarajan, M. PCR-RFLP and sequence analysis of 12S and 16S rRNA mitochontrial genes of grey mullets from East coast of India. Indian J. Geo Mar. Sci. 2011, 40, 529–534. [Google Scholar]
  70. Kumar, C.P.; John, B.A.; Khan, S.A.; Lyla, P.S.; Murugan, S.; Rozihan, M.; Jalal, K.C.A. Efficiency of universal barcode gene (Coxi) on morphologically cryptic Mugilidae fishes delineation. Trends Appl. Sci. Res. 2011, 6, 1028–1036. [Google Scholar]
  71. Karna, S.K.; Mukherjee, M.; Suresh, V.R. Length–weight relationships for four mullets from the Chilika lagoon, East coast of India. J. Appl. Ichthyol. 2018, 34, 747–749. [Google Scholar] [CrossRef]
  72. Jones, S.; Kumaran, M. Fishes of the Laccadive Archipelago; The Nature Conservation and Aquatic Sciences Service: Trivandrum, India, 1980; 760p. [Google Scholar]
  73. Hasan, A.; Siddiqui, P.J.A.; Amir, S.A.; Durand, J.-D. DNA Barcoding of Mullets (Family Mugilidae) from Pakistan Reveals Surprisingly High Number of Unknown Candidate Species. Diversity 2021, 13, 232. [Google Scholar] [CrossRef]
  74. Alavi-Yeganeh, M.S.; Ghasemzadeh, J.; Kouhi, S.; Durand, J.-D. The squaretail mullet Ellochelon vaigiensis (Quoy & Gaimard, 1825) a complex of cryptic species? Contrib. Zool. 2023, 1, 1–17. [Google Scholar] [CrossRef]
  75. Tridge. Import Value Trend of HS Code 030389 (Grey Mullet) from All Countries to India. Available online: https://www.tridge.com/trades/data?code=030389&flow=i&reporter=IN (accessed on 24 July 2023).
  76. Smith, A. Illustrations of the Zoology of South Africa; Consisting Chiefly of Figures and Descriptions of the Objects of Nat. Hist. Collected during an Expedition into the Interior of South Africa, in the Years 1834, 1835, and 1836; Fitted out by "The Cape of Good Hope Association for Exploring Central Africa"; Smith, Elder and Co.: London, UK, 1838–1847; Volume 4, 31p. [Google Scholar] [CrossRef]
  77. Whitfield, A.K.; Panfili, J.; Durand, J.D. A global review of the cosmopolitan flathead mullet Mugil cephalus Linnaeus 1758 (Teleostei: Mugilidae), with emphasis on the biology, genetics, ecology and fisheries aspects of this apparent species complex. Rev. Fish Biol. Fish. 2012, 22, 641–681. [Google Scholar] [CrossRef]
  78. Shen, K.N.; Jamandre, B.W.; Hsu, C.C.; Tzeng, W.N.; Durand, J.D. Plio-Pleistocene Sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evol. Biol. 2011, 11, 83. [Google Scholar] [CrossRef] [PubMed]
  79. Shen, K.N.; Chang, C.W.; Durand, J.D. Spawning segregation and philopatry are major prezygotic barriers in sympatric cryptic Mugil cephalus species. Comptes Rendus Biol. 2015, 338, 803–811. [Google Scholar] [CrossRef]
  80. Dhar, B.; Ghosh, S.K. Genetic assessment of ornamental fish species from North East India. Gene 2015, 555, 382–392. [Google Scholar] [CrossRef]
  81. Dor, L.; Shirak, A.; Rosenfeld, H.; Meiri-Ashkenazi, I.; Rubinstein, G.; Seroussi, E.; Weller, J.I.; Ron, M. Genetic Stock Identification of the Flathead Grey Mullet (Mugil cephalus) in Lake Tiberias Based on Parent Offspring Relationship. Isr. J. Aquac. 2018, 70, 2-11. IJA_70.2018.1452. [Google Scholar] [CrossRef]
  82. Durand, J.D.; Chen, W.J.; Shen, K.N.; Fu, C.; Borsa, P. Genus-level taxonomic changes implied by the mitochondrial phylogeny of grey mullets (Teleostei: Mugilidae). Comptes Rendus Biol. 2012, 335, 687–697. [Google Scholar] [CrossRef]
  83. Khedkar, G.D.; Jamdade, R.; Naik, S.; David, L.; Haymer, D. DNA barcodes for the fishes of the Narmada, one of India’s longest rivers. PLoS ONE 2014, 9, e101460. [Google Scholar] [CrossRef]
  84. Reddy, P.S.R. Biosystematic Studies in Mullets (Family: Mugilidae) of Porto Novo, Tamil Nadu, South India. Ph.D. Thesis, Annamalai University, Chidambaram, India, 1977. [Google Scholar]
  85. Weber, M.; de Beaufort, L.F. The Fishes of the Indo-Australian Archipelago, Heteromi, Solenichthyes, Synentognathi, Percesoces, Labyrinthici, Microcyprini; EJ Brill Ltd.: Leiden, The Netherlands, 1922; Volume 4, 409p. [Google Scholar]
Diversity 15 01193 g001aDiversity 15 01193 g001b
Figure 1. Maps showing locations of sample collection in southern peninsular India.
Figure 1. Maps showing locations of sample collection in southern peninsular India.
Diversity 15 01193 g001aDiversity 15 01193 g001b
Diversity 15 01193 g002
Figure 2. The maximum likelihood phylogenetic tree of the family Mugilidae from India (Arabic numerals inside the circles represent “species groups” found in India, and these same numbers are also depicted in the matrix diagram (Figure 3). Sequences originating from the Indian region are denoted with “*” in the tree).
Figure 2. The maximum likelihood phylogenetic tree of the family Mugilidae from India (Arabic numerals inside the circles represent “species groups” found in India, and these same numbers are also depicted in the matrix diagram (Figure 3). Sequences originating from the Indian region are denoted with “*” in the tree).
Diversity 15 01193 g002
Diversity 15 01193 g003
Figure 3. Matrix diagram representing pairwise genetic distances among COI sequences of Indian species groups. (Arabic numerals in the green squares are the same species group number depicted in Figure 2, decimal numbers in the yellow squares represent the fraction of the maximum possible genetic distance between the corresponding species groups).
Figure 3. Matrix diagram representing pairwise genetic distances among COI sequences of Indian species groups. (Arabic numerals in the green squares are the same species group number depicted in Figure 2, decimal numbers in the yellow squares represent the fraction of the maximum possible genetic distance between the corresponding species groups).
Diversity 15 01193 g003
Diversity 15 01193 g004
Figure 4. The maximum likelihood phylogenetic tree constructed using the newly generated sequences as part of our study.
Figure 4. The maximum likelihood phylogenetic tree constructed using the newly generated sequences as part of our study.
Diversity 15 01193 g004
Table 1. Details of species, locations, and barcode length, and GenBank accession number of newly generated sequences.
Table 1. Details of species, locations, and barcode length, and GenBank accession number of newly generated sequences.
Species NameFishing LocationsLatitude (N)Longitude (E)COI
Sequence Length (bp)		GenBank Accession
Crenimugil buchanani (Bleeker 1853)Vellar, Tamil Nadu11.49879.776645MW137482
Crenimugil buchananiVellar, Tamil Nadu11.49879.776644MW137480
Crenimugil buchananiVellar, Tamil Nadu11.49879.776644MW137481
Crenimugil cf. seheli sp. A Muthalapozhi, Kerala8.63176.783582MN728321
Crenimugil cf. seheli sp. AMuthalapozhi, Kerala8.63176.783582MN728322
Crenimugil cf. seheli sp. BCochin, Kerala9.966776.2333676MW137486
Crenimugil cf. seheli sp. BMunambam, Kerala10.17876.169582MN728320
Ellochelon sp. BVellar, Tamil Nadu11.49879.776645MW137487
Ellochelon sp. BVellar, Tamil Nadu11.49879.776644MW137488
Ellochelon sp. BVellar, Tamil Nadu11.49879.776643MW137489
Mugil cf. cephalusVellar, Tamil Nadu11.49879.776627MW137496
Mugil cf. cephalusVellar, Tamil Nadu11.49879.776645MW137497
Mugil cf. cephalusVellar, Tamil Nadu11.49879.776644MW137498
Mugil cf. cephalusVellar, Tamil Nadu11.49879.776645MW137499
Mugil cf. cephalusVellar, Tamil Nadu11.49879.776646MW137500
Mugil cf. cephalusCochin, Kerala9.966776.2333676MW137495
Mugil cf. cephalusCochin, Kerala9.966776.2333644MW137494
Mugil cf. cephalusPoyya, Kerala10.221 76.234582MN728324
Mugil cf. cephalusKorapuzha, Kerala11.39675.745582MN728325
Mugil cf. cephalusPoyya, Kerala10.221 76.234582MN728326
Mugil cf. cephalusKattampally, Kerala11.937 75.376582MN728327
Osteomugil cf. perusiiAshtamudi, Kerala8.95976.577582MN728329
Osteomugil cf. perusiiPoyya, Kerala10.221 76.234582MN728330
Osteomugil cf. perusiiFort Kochi, Kerala9.96376.237582MN728331
Osteomugil cf. perusiiMadakkara, Kerala,12.2167275.130238582MN728332
Osteomugil sp. DVellar, Tamil Nadu11.49879.776676MW137515
Osteomugil sp. DVellar, Tamil Nadu11.49879.776653MW137514
Osteomugil sp. DVellar, Tamil Nadu11.49879.776655MW137516
Osteomugil sp. DThrikkaripur, Kerala12.13875.16582MN728328
Planiliza cf. macrolepis sp. HVellar, Tamil Nadu11.49879.776679MW137525
Planiliza cf. macrolepis sp. HVellar, Tamil Nadu11.49879.776658MW137524
Planiliza cf. macrolepis sp. HVellar, Tamil Nadu11.49879.776658MW137523
Planiliza cf. macrolepis sp. HVellar, Tamil Nadu11.49879.776658MW137522
Planiliza cf. macrolepis sp. HParavoor, Kerala8.83576.667582MN728317
Planiliza cf. macrolepis sp. HParavoor, Kerala8.83576.667582MN728318
Planiliza cf. macrolepis sp. HVellar, Tamil Nadu11.41875.734582MN728319
Planiliza sp. DVellar, Tamil Nadu11.49879.776652MW137518
Planiliza sp. DCochin, Kerala9.966776.2333678MW137535
Planiliza sp. DCochin, Kerala9.966776.2333644MW137544
Planiliza sp. DCochin, Kerala9.966776.2333644MW137540
Planiliza sp. DCheruvathur, Kerala12.20375.129582MN728302
Planiliza sp. DValapattanam, Kerala12.0475.49582MN728303
Planiliza sp. DKayamkulam, Kerala9.16176.46582MN728304
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728305
Planiliza sp. DThrikkaripur, Kerala12.14175.172582MN728306
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728307
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728308
Planiliza sp. DEdakochi, Kerala9.91676.291582MN728309
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728310
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728311
Planiliza sp. DKorapuzha, Kerala11.39675.745582MN728312
Planiliza sp. DKayamkulam, Kerala9.16176.46582MN728313
Planiliza sp. DCochin, Kerala9.86376.32582MN728314
Planiliza sp. DCochin, Kerala9.86376.32582MN728315
Planiliza sp. DFort Kochi, Kerala9.96376.237582MN728316
Planiliza subviridisVellar, Kerala11.49879.776652MW137547
Planiliza subviridisCochin, Kerala11.49879.776644MW137546
Planiliza subviridisCochin, Kerala11.49879.776665MW137545
Planiliza subviridisCochin, Kerala11.49879.776644MW137548
Planiliza subviridisVellar, Tamil Nadu11.49879.776643MW137551
Planiliza subviridisVellar, Tamil Nadu11.49879.776644MW137550
Planiliza subviridisVellar, Tamil Nadu11.49879.776644MW137566
Planiliza subviridisVellar, Tamil Nadu11.49879.776652MW137549
Planiliza subviridisCochin, Kerala9.86376.32646MW137552
Planiliza subviridisKattampally, Kerala11.937 75.376582MN728289
Planiliza subviridisVarapuzha, Kerala10.07476.239582MN728290
Planiliza subviridisCheliya, Kerala12.0475.49582MN728291
Planiliza subviridisThrikkaripur, Kerala12.13875.16582MN728292
Planiliza subviridisKayamkulam, Kerala9.16176.46582MN728293
Planiliza subviridisKorapuzha, Kerala11.39675.745582MN728294
Planiliza subviridisParavoor, Kerala8.83576.667582MN728295
Planiliza subviridisThrikkaripur, Kerala12.13875.16582MN728296
Planiliza subviridisFort Kochi, Kerala9.96376.237582MN728297
Planiliza subviridisPoyya, Kerala10.221 76.234582MN728298
Planiliza subviridisKattampally, Kerala11.937 75.376582MN728299
Planiliza subviridisKorapuzha, Kerala11.39675.745582MN728300
Planiliza subviridisKayamkulam, Kerala9.16176.46582MN728301
Plicomugil labiosusAgatti, Lakshadweep10.85772.1959582MN728323
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Rajan, R.; Durand, J.-D.; Thomas, L.; Sidharthan, A.; Rahman, M.A.U.; Xavier, B.; Raghavan, R. Barcoding Mullets (Mugilidae): Genetic Characterization of Exploited Species in Southern Peninsular India. Diversity 2023, 15, 1193. https://doi.org/10.3390/d15121193

AMA Style

Rajan R, Durand J-D, Thomas L, Sidharthan A, Rahman MAU, Xavier B, Raghavan R. Barcoding Mullets (Mugilidae): Genetic Characterization of Exploited Species in Southern Peninsular India. Diversity. 2023; 15(12):1193. https://doi.org/10.3390/d15121193

Chicago/Turabian Style

Rajan, Rahul, Jean-Dominique Durand, Liju Thomas, Arya Sidharthan, M. Ashiq Ur Rahman, Bibin Xavier, and Rajeev Raghavan. 2023. "Barcoding Mullets (Mugilidae): Genetic Characterization of Exploited Species in Southern Peninsular India" Diversity 15, no. 12: 1193. https://doi.org/10.3390/d15121193

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop