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RAPID COMMUNICATION
Complete mitochondrial genome of Chroicocephalus brunnicephalus from India:
phylogeny with other Larids
Shantanu Kundu
a
, Kaomud Tyagi
a
, Imran Alam
b
, Gopinathan Maheswaran
b
, Vikas Kumar
a
and
Kailash Chandra
a,b
a
Centre for DNA Taxonomy, Molecular Systematics Division, Zoological Survey of India, Kolkata, India;
b
Bird Section, Zoological Survey of
India, Kolkata, India
ABSTRACT
The complete mitogenome sequence of the brown-headed gull, Chroicocephalus brunnicephalus was
determined in this study. The 16,771bp genome consists of 13 protein-coding genes (PCGs), two ribo-
somal RNA (rRNA) genes, and 22 transfer RNA (tRNA) genes, and a control region (CR). The decoded
mitogenome was AT-rich (54.77%) with nine overlapping and 17 intergenic spacer regions. Most of the
PCGs were started by a typical ATG initiation codon except for cox1 and nad3. Further, the usual ter-
mination codons (AGG, TAG, TAA, and AGA) were used by 11 PCGs except for cox3 and nad4. The con-
catenated PCGs based Bayesian phylogeny clearly discriminates all the Laridae species and reflects the
sister relationship of C. brunnicephalus with C. ridibundus. The present mitogenome-based phylogeny
was congruent with the earlier hypothesis and confirmed the evolutionary position of the brown-
headed gull as masked species. The generated mitogenome of C. brunnicephalus is almost identical to
the previously generated mitogenome from China except for two base pairs in CR. To visualize the
population structure of this migratory species, we propose more sampling from different geographical
locations and the generation of additional molecular data to clarify the reality.
ARTICLE HISTORY
Received 19 August 2020
Accepted 13 December 2020
KEYWORDS
Gulls; migratory species;
mitogenome; phyl-
ogeny; evolution
1. Introduction
The family Laridae (order: Charadriiformes) comprises 105
known species under 20 genera globally (BirdLife
International 2020). Among them, 38 species under 17 gen-
era were recorded from Indian coastal or inland (Praveen
et al. 2020). They are medium to large-sized shorebirds, com-
monly known as gulls. Typically they are white or gray in
color with webbed feet and have typical harsh wailing calls.
Among all extant gulls, the brown-headed gull
Chroicocephalus brunnicephalus usually migrate from China to
their wintering localities in Thailand and Cambodia; while
Bangladesh, India, Myanmar, and Vietnam being their major
stopover locations during such migrations. They can travel an
average distance of about 2400 km from their breeding
grounds and take one to two weeks to cover this distance
(Ratanakorn et al. 2012). Due to habitat loss, over-fishing, and
other anthropogenic pressures, the population trend of many
gulls is declining throughout the world including India (Aarif
et al. 2014). Furthermore, C. brunnicephalus is also reported
to be a host of highly pathogenic avian influenza H5N1 virus
and could be a potential carrier for the outbreak within
Southeast Asian countries and act as an environmental bio-
indicator (Ratanakorn et al. 2012; Hasan et al. 2014).
Owing to the convergent plumage evolution, the taxo-
nomic approach often flunks to resolve the phylogenetic rela-
tionship of Charadriiformes birds (Crochet et al. 2000). Later
on, the genetic analyses evidenced that, the order
Charadriiformes can be classified into three major clades
(Paton and Baker 2006; Fain and Houde 2007; Livezey 2010).
However, the evolutionary relationship of this group is still
perplexing while examining in-depth phylogenetic analysis.
Both mitochondrial and nuclear genetic information were
well studied to know the systematics status, evolutionary
relationships, and population structures of Charadriiformes
birds (Liebers et al. 2001; Crochet et al. 2003; Ericson et al.
2003; Paton et al. 2003; Thomas et al. 2004; van Tuinen et al.
2004; Pons et al. 2005; Baker et al. 2007). The comparative
genomics is also employed for estimating the genetic vari-
ability, substitution pattern, phylogenetic relationship, and
evolution of avifauna (van Tuinen et al. 2001; Paton et al.
2002; Backstr€
om et al. 2008; Hackett et al. 2008;K
€
unstner
et al. 2010). As of now, 47 complete mitochondrial genomes
of Charadriiformes birds are available in the GenBank data-
base. Among them, 13 mitogenomes of 11 Laridae species
were generated from different geographical regions (Slack
et al. 2007; Ryu and Hwang 2012; Yang et al. 2012,2016,
2017; Yoon et al. 2015; Dong et al. 2016; Kim and Park 2016;
CONTACT Vikas Kumar vikaszsi77@gmail.com Centre for DNA Taxonomy, Molecular Systematics Division, Zoological Survey of India, M Block, New
Alipore, Kolkata 700053, India
Supplemental data for this article is available online at https://doi.org/10.1080/23802359.2020.1866448.
ß2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits
unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
MITOCHONDRIAL DNA PART B
2021, VOL. 6, NO. 2, 339–343
https://doi.org/10.1080/23802359.2020.1866448
Anmarkrud and Lifjeld 2017; Skujina et al. 2019). The analysis
of the complete mitogenomes was also evidenced to charac-
terize various genomic traits within protein-coding genes
(PCGs), ribosomal RNA (rRNA), transfer RNA (tRNA), and con-
trol region (CR) as well as to detect gene order evolution in
birds (Bensch and H€
arlid 2000; Crochet and Desmarais 2000;
Ruokonen and Kvist 2002; Pacheco et al. 2011). Hence, this
study is aimed to generate the complete mitochondrial gen-
ome of the brown-headed gull from India and estimate the
phylogeny with other Laridae species to determine the evolu-
tionary relationships.
2. Materials and methods
A naturally dead adult specimen of C. brunnicephalus was col-
lected on 27 February 2019 from the seashore of Coringa
Wildlife Sanctuary (16.58 N 82.30 E) in Andhra Pradesh, India
(Figure 1(A)). As the sample was naturally dead, no prior per-
mission was acquired for this biological sampling. The live
photograph of the same species was captured from the same
locality. The country-level map has been downloaded from
the spatial data platform and overlaying by DIVA-GIS 7.5 soft-
ware (http://www.diva-gis.org). The muscle tissue was col-
lected from the carcass specimen in a sterile condition and
stored in 70% ethanol at 80 C in the National Zoological
Collections of Bird Section, Zoological Survey of India, Kolkata
under voucher No. 41301/AVES.
The collected tissue sample was thoroughly chopped by
the surgical blade and re-suspended in 200 ll of buffer
(50 mM Tris–HCl, 25 mM of EDTA, and 150 mM NaCl), with the
addition of 20 ll of proteinase K (20 mg/ml) followed by incu-
bation at 56 C for overnight. The sample was further reli-
giously vortex with 10 ml buffer (0.32 M Sucrose, 1 mM EDTA,
10 mM Tris–HCl) and centrifuged at 700 gfor 5 min at 4 C
to remove nuclei and cell debris. The supernatant was col-
lected in 1.5 ml Eppendorf tubes and centrifuged at
12,000 gfor 10 min at 4 C to precipitate the mitochondrial
pellet. The mitochondrial DNA was extracted by Qiagen
DNeasy Blood & Tissue Kit (QIAGEN Inc., Germantown, MD)..
The complete mitochondrial genome was obtained com-
mercially and the high-quality paired-end data was
assembled through NOVOPlasty version 2.6.7 with default
parameters (Dierckxsens et al. 2017). The genome library was
sequenced using the Illumina platform (2 150 bp PE chem-
istry), to generate 6 GB data (Illumina, Inc, San Diego, CA).
The raw reads were screened using cutadapt tool (http://
code.google.com/p/cutadapt/) and low-quality bases were
trimmed with a cutoff of Phred quality score (Q score ¼20).
The cox1 sequence of the same species (accession no.
NC_018548/JX155863) was used as a reference seed
sequence for the present assembly. To confirm the assembly,
a similarity search was carried out in the GenBank database
using BLASTn version 2.2.28 search (https://blast.ncbi.nlm.nih.
gov) algorithm.
The spherical representation of the generated mitoge-
nome of C. brunnicephalus was plotted by CGView Server
(http://stoth ard.afns.ualbe rta.ca/cgview_server/) with default
parameters (Grant and Stothard 2008). The strand direction
and arrangements of each PCG, tRNA, rRNA, and CR were
checked through MITOS version 806 online web server
(http://mitos.bioinf.uni-leipzig.de) (Bernt et al. 2013). The
overlapping regions and intergenic spacers between the
neighbor genes were counted manually through Microsoft
Excel. The sequences of PCGs were translated into the puta-
tive amino acid sequences on the basis of the vertebrate
mitochondrial genetic code. The initiation and termination
codons were identified in ClustalX using other publicly avail-
able reference sequences of Laridae (Thompson et al. 2003).
The mitogenome sequence was submitted to the GenBank
database through the Bankit submission tool. The mitoge-
nome size and nucleotide composition were calculated using
MEGA version 6.0 (Tamura et al. 2013).
On the basis of homology search in the Refseq database
(https://www.ncbi.nlm.nih.gov/refse q/), 11 Laridae species
mitogenomes were downloaded from GenBank and incorpo-
rated in the dataset for their phylogenetic relationships. The
PCGs were aligned individually by codons using MAFFT algo-
rithm in TranslatorX with L-INS-i strategy with GBlocks param-
eters (Abascal et al. 2010). The dataset of all PCGs was
concatenated using SequenceMatrix version 1.7.84537
(Vaidya et al. 2011). The best suitable model (GTR þGþI) for
phylogenetic analysis was calculated by PartitionFinder 2
(Lanfear et al. 2016) at CIPRES Science Gateway version 3.3
(Miller et al. 2015). The Bayesian analysis (BA) was performed
through Mr. Bayes version 3.1.2 and the metropolis-coupled
Markov Chain Monte Carlo (MCMC) was run for 100,000,000
generations with sampling at every 100th generation and
25% of samples were discarded as burn-in (Ronquist and
Huelsenbeck 2003). The BA phylogeny was further illustrated
in iTOL version 4 (https://itol.embl.de/login.cgi) and edited
with Adobe Photoshop CS version 8.0. The database
sequence of Gallus gallus (order Galliformes) was as out-
group taxa in the phylogenetic analysis.
3. Results and discussion
The complete mitochondrial genome of C. brunnicephalus
was determined by using next-generation sequencing
approach. The total length of the decoded mitogenome was
16,771 bp and deposited with the accession number
(MT876573/NC_050864) in the GenBank database. The com-
plete mitogenome contains 13 PCGs, 22 tRNAs, two rRNAs,
and a CR as depicted in other avian mitogenomes (Figure
1(B),Table S1). A total of nine genes (nad6 and eight tRNAs)
were located on the light strand, while the other genes were
encoded on the heavy strand. The overall base-composition
of this mitogenome was 30.72% A, 14.13% G, 31.10% C, and
24.04% T. The AT and GC content of the complete mitoge-
nome was 54.77 and 45.23%, respectively. A total of nine
overlapping regions with a total length of 34 bp were identi-
fied. These sequences varied in length (1–10 bp) with the lon-
gest overlapping region present between ATP synthase F0
subunit 8 (atp8) and ATP synthase F0 subunit 6 (atp6).
Further, the intergenic spacers spread over 17 regions rang-
ing from 1 to 19 bp with a total length of 68 bp. The longest
spacer (19 bp) occurred between NADH dehydrogenase
340 S. KUNDU ET AL.
subunit 5 (nad5) and Cytochrome b (Cytb)(Table S1). Most of
the PCGs were started by the typical ATG initiation codon
with an exception in Cytochrome oxidase subunit I (cox1)
with GTG and NADH dehydrogenase subunit 3 (nad3) with
ATT. The 11 PCGs used usual termination codons (AGG, TAG,
TAA, and AGA), except for Cytochrome oxidase subunit III
(cox3) and NADH dehydrogenase subunit 4 (nad4) with
incomplete termination codon (T) (Table S1).
The mitogenome based BA phylogeny clearly discrimi-
nates all the studied Laridae species with high posterior
probability supports (Figure 1(C)). Both Indian and Chinese C.
brunnicephalus sequences were cohesively clustered in the
BA tree and reflected the sister relationship with the Black-
headed gull, Chroicocephalus ridibundus. The C. brunnicepha-
lus was thought to be a valid species under genus Larus
from long back and later on shifted under Chroicocephalus
genus based on the mitochondrial markers based phylogeny
(Pons et al. 2005). This taxonomic revision was further
accorded by the subsequent studies (Sternkopf 2011; Liebers-
Helbig 2013). The present complete mitochondrial genome-
Figure 1. (A) Map showing the collection locality of C. brunnicephalus from the southern coast of India. (B) The spherical representation of mitochondrial genome
of C. brunnicephalus. Direction of gene transcription is indicated by arrows. PCGs are shown as blue arrows, rRNA genes as coral arrows, tRNA genes as orchid arrows,
and non-coding control region as mint rectangle. The GC-skew is plotted using green and violet color sliding window as the deviation from the average in the com-
plete mitogenome. The species photograph was taken by the third author (G.M.) (C) The BA phylogeny based on the concatenated nucleotide sequences of 13
PCGs showing the evolutionary relationship of the studied taxa with other Laridae species. The posterior probability support values were superimposed with each
node. The figure was edited with the representative species photograph acquired from the internet using Adobe Photoshop CS version 8.0.
MITOCHONDRIAL DNA PART B 341
based phylogeny elucidates congruent results with the earlier
hypothesis (Pons et al. 2005) and confirmed their evolution-
ary position as masked species.
The genetic applications are largely employed in the con-
servation of avifauna around the world (Haig et al. 2011). It is
also detected that the genetic composition of birds is often
altered linked with their fragmented habitats (Brown et al.
2004). Further, it is also noticed that the migratory species
acquired their energy via mitochondrial adaptations and oxi-
dative phosphorylation during their locomotion (Toews et al.
2014). It is also evident that locomotion plays an important
role in the evolution of mtDNA and independently evolves
different lineages (Pulido 2007; Shen et al. 2009). The
molecular study further suggested the gene flow controlling
the expression of migratory behavior of birds (Mueller et al.
2011; Pons et al. 2014). This analysis elucidates that the
nucleotide composition of the Indian C. brunnicephalus mito-
genome, sampled from the Southern coast is almost identical
to the Chinese mitogenome (accession no. NC_018548/
JX155863) except for two base pairs in CR. The genetic infor-
mation of these two isolates is important and could be
adopted for population genetics studies of this Laridae spe-
cies in near future. However, we suggest more sampling
from different geographical locations and subsequent gener-
ation of more molecular data to clarify the mitochondrial
introgression and function of this migratory species.
Acknowledgments
We are thankful to the Director of Zoological Survey of India (ZSI),
Ministry of Environment, Forest and Climate Change (MoEF&CC), Govt. of
India for providing necessary molecular facilities and support for the
study. The first author (SK) acknowledges the fellowship grant received
from the Council of Scientific and Industrial Research (CSIR) Senior
Research Associateship (Scientists’Pool Scheme) Pool No. 9072-A. We
thank Avas Pakrashi and Pronomay Karmakar for analytical help.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
The research is funded by the National Faunal Genome Resources (NFGR)
funding of Zoological Survey of India (ZSI), Kolkata, Ministry of
Environment, Forest and Climate Change (MoEF&CC), New Delhi, India.
The funders had no role in study design, data collection and analysis, or
preparation of the manuscript.
ORCID
Shantanu Kundu http://orcid.org/0000-0002-5488-4433
Kaomud Tyagi http://orcid.org/0000-0003-1064-9826
Imran Alam http://orcid.org/0000-0003-3577-966X
Gopinathan Maheswaran http://orcid.org/0000-0003-2496-9556
Vikas Kumar http://orcid.org/0000-0002-0215-0120
Kailash Chandra http://orcid.org/0000-0001-9076-5442
Data availability statement
The complete mitochondrial genome data that support the findings of
this study are openly available in NCBI GenBank database at (https://
www.ncbi.nlm.nih.gov) with the accession number (MT876573/NC_
050864) which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
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