Molecular identification of Brachygenys and Haemulon species (Perciformes: Haemulidae) from the Brazilian coast

The fishes of the Haemulidae family are currently allocated to 19 genera with a worldwide distribution in the tropical and subtropical waters of the world’s oceans. Brachygenys and Haemulon are important genera of reef fish in Brazil, as they occur in large shoals, which are both ecologically and commercially valuable. This study identified the Brazilian species of the genera Brachygenys and Haemulon using DNA barcodes. While we found only a single lineage in Brachygenys chrysargyrea, Haemulon melanurum, H. parra, and H. squamipinna, more than one molecular operational taxonomic unit (MOTU) was identified in H. atlanticus, H. aurolineatum, and H. plumieri, indicating the possible existence of discrete populations or cryptic species.

Keywords:
Barriers; DNA barcoding; Marine fish; Species delimitation; Western Atlantic

Authorship

Najila Nolie Catarine Dantas Cerqueira

Laboratório de Biologia e Genética de Peixes, Departamento de Biologia Estrutural e Funcional, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho IBB/UNESP, R. Prof. Dr. Antonio Celso Wagner Zanin, 250, Distrito de Rubião Junior, 18618-689 Botucatu, SP, Brazil. (NNCDC) najila.nolie@unesp.br (corresponding author); (VPC) cruzvp@outlook.com; (FF) f.foresti@unesp.br; (CO) claudio.oliveira@unesp.br.Universidade Estadual Paulista Júlio de Mesquita Filho IBB/UNESPBrazilBotucatu, SP, BrazilLaboratório de Biologia e Genética de Peixes, Departamento de Biologia Estrutural e Funcional, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho IBB/UNESP, R. Prof. Dr. Antonio Celso Wagner Zanin, 250, Distrito de Rubião Junior, 18618-689 Botucatu, SP, Brazil. (NNCDC) najila.nolie@unesp.br (corresponding author); (VPC) cruzvp@outlook.com; (FF) f.foresti@unesp.br; (CO) claudio.oliveira@unesp.br.

https://orcid.org/0000-0003-3200-0630

Matheus Marcos Rotundo

Acervo Zoológico da Universidade de Santa Cecília AZUSC, Universidade Santa Cecília UNISANTA, Rua Oswaldo Cruz, 266, Boqueirão, 11045-907 Santos, SP, Brazil. (MMR) mmrotundo@unisanta.br.Universidade Santa Cecília UNISANTABrazilSantos, SP, BrazilAcervo Zoológico da Universidade de Santa Cecília AZUSC, Universidade Santa Cecília UNISANTA, Rua Oswaldo Cruz, 266, Boqueirão, 11045-907 Santos, SP, Brazil. (MMR) mmrotundo@unisanta.br.

https://orcid.org/0000-0003-1886-5320

Alexandre Pires Marceniuk

Museu Paraense Emílio Goeldi – MPEG, Avenida Governador Magalhães Barata, Nazaré, 66040-170 Belém, PA, Brazil. (APM) a_marceniuk@hotmail.com.>Museu Paraense Emílio GoeldiBrazilBelém, PA, BrazilMuseu Paraense Emílio Goeldi – MPEG, Avenida Governador Magalhães Barata, Nazaré, 66040-170 Belém, PA, Brazil. (APM) a_marceniuk@hotmail.com.

https://orcid.org/0000-0003-4286-0482

Vanessa Paes da Cruz

https://orcid.org/0000-0002-2450-8701

Fausto Foresti

https://orcid.org/0000-0002-0862-0445

Claudio Oliveira

https://orcid.org/0000-0002-7010-8880

Edited-by

Fernando Gibran

Correspondence

Najila Nolie C. Dantas Cerqueira najila.nolie@unesp.br

Author's Contribution

Najila Nolie Catarine Dantas Cerqueira: Conceptualization, Formal analyses, Methods, Writing-original draft, Writing-review and editing.

Matheus Marcos Rotundo: Conceptualization, Data curation, Writing-review and editing.

Alexandre Pires Marceniuk: Conceptualization, Data curation, Writing-review and editing.

Vanessa Paes da Cruz: Conceptualization, Software, Writing-original draft, Writing-review and editing.

Fausto Foresti: Conceptualization, Project administration, Resources, Writing-review and editing.

Claudio Oliveira: Conceptualization, Project administration, Resources, Supervision, Writing-original draft, Writing-review and editing.

Competing Interests

The authors declare no competing interests.

Ethical Statement

The species were sampled in accordance with Brazilian legislation, as regulated by the National Council for the Control of Animal Experimentation (CONCEA) and authorized by the Ethics Committee on the Use of Animals (CEUA) of the Biosciences Institute at UNESP through its (protocol 1057/2017).

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (3)
Tables (2)

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FIGURE 1 |
Species of the genera Haemulon and Brachygenys collected off the coast of Brazil during this study. A. Haemulon aurolineatum (16.2 cm of Total Length, TL); B. H. melanurum (18.3 cm of TL); C. H. parra (21.7 cm of TL); D. H. squamipinna (15.9 cm of TL); E. H. plumieri (23.5 cm of TL); F. H. atlanticus (16.1 cm of TL); G. Brachygenys chrysargyrea (16.0 cm of TL).

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FIGURE 2 |
The Maximum Likelihood tree of the Haemulon and Brachygenys specimens, based on the sequences of the mitochondrial cytochrome c oxidase subunit I gene under the TRN+G model. The numbers at each branch indicate the bootstrap values (1000 pseudoreplicates) and those between parentheses are the number of specimens analyzed. The species delimitation methods were ABGD, PTP, and GMYC (see Material and Methods section).

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FIGURE 3 |
Haplotype networks of the three Haemulon species in which multiple MOTUs were identified. The dashes represent mutational steps. The size of the circle representing each haplotype is proportional to the number of individuals with that haplotype. The black dots represent missing haplotypes. A. H. steindachneri = Haemulon steindachneri (eastern Pacific); H. atlanticus B = specimens from Colombia, Guatemala, and Venezuela; H. atlanticus A = specimens from Brazil and Colombia; B. H. aurolineatum A = specimens from Bermuda; H. aurolineatum B = specimens from Bermuda; H. aurolineatum C = specimens from the United States; H. aurolineatum D = specimens from Belize, Brazil, Colombia, Jamaica, Venezuela, and the United States; and C. H. plumieri C = specimens from Brazil and Puerto Rico; H. plumieri B = specimens from the United States; H. plumieri A = specimens from the Bahamas, Belize, Haiti, Mexico, Puerto Rico, and the United States.

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TABLE 1 |
Pairwise K2P genetic distances between the Brachygenys and Haemulon species (below the diagonal) and standard errors (above the diagonal). The numbers in bold type represent the intraspecific K2P genetic distances and their standard errors.

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TABLE 2 |
Pairwise K2P distances between Brachygenys and Haemulon genetic lineages (below the diagonal) and standard errors (above the diagonal). The numbers in bold type represent the intraspecific K2P genetic distances. + Only one sample available. The species identified by letters correspond to the distribution of the specimens as described in the article.

FIGURE 1 | Species of the genera Haemulon and Brachygenys collected off the coast of Brazil during this study. A. Haemulon aurolineatum (16.2 cm of Total Length, TL); B. H. melanurum (18.3 cm of TL); C. H. parra (21.7 cm of TL); D. H. squamipinna (15.9 cm of TL); E. H. plumieri (23.5 cm of TL); F. H. atlanticus (16.1 cm of TL); G. Brachygenys chrysargyrea (16.0 cm of TL).

FIGURE 2 | The Maximum Likelihood tree of the Haemulon and Brachygenys specimens, based on the sequences of the mitochondrial cytochrome c oxidase subunit I gene under the TRN+G model. The numbers at each branch indicate the bootstrap values (1000 pseudoreplicates) and those between parentheses are the number of specimens analyzed. The species delimitation methods were ABGD, PTP, and GMYC (see Material and Methods section).

FIGURE 3 | Haplotype networks of the three Haemulon species in which multiple MOTUs were identified. The dashes represent mutational steps. The size of the circle representing each haplotype is proportional to the number of individuals with that haplotype. The black dots represent missing haplotypes. A. H. steindachneri = Haemulon steindachneri (eastern Pacific); H. atlanticus B = specimens from Colombia, Guatemala, and Venezuela; H. atlanticus A = specimens from Brazil and Colombia; B. H. aurolineatum A = specimens from Bermuda; H. aurolineatum B = specimens from Bermuda; H. aurolineatum C = specimens from the United States; H. aurolineatum D = specimens from Belize, Brazil, Colombia, Jamaica, Venezuela, and the United States; and C. H. plumieri C = specimens from Brazil and Puerto Rico; H. plumieri B = specimens from the United States; H. plumieri A = specimens from the Bahamas, Belize, Haiti, Mexico, Puerto Rico, and the United States.

TABLE 1 | Pairwise K2P genetic distances between the Brachygenys and Haemulon species (below the diagonal) and standard errors (above the diagonal). The numbers in bold type represent the intraspecific K2P genetic distances and their standard errors.

Species	1	2	3	4	5	6	7	8	9	10
1. Brachygenys jessiae	-	0.0188	0.0182	0.0178	0.0185	0.0207	0.0177	0.0206	0.0202	0.0212
2. B. chrysargyrea	0.1376	0.004±0.001	0.0169	0.0201	0.0168	0.0199	0.0179	0.0186	0.0186	0.0178
3. B. californiensis	0.1398	0.1269	0.002±0.001	0.0156	0.0157	0.0176	0.0176	0.0169	0.0173	0.0164
4. Haemulon aurolineatum	0.1502	0.1643	0.1185	0.022±0.003	0.0146	0.0156	0.0157	0.0157	0.0145	0.0155
5. H. plumieri	0.1553	0.1365	0.1258	0.1192	0.027±0.005	0.0156	0.0169	0.0161	0.0149	0.0167
6. H. melanurum	0.1608	0.1604	0.1332	0.1128	0.1223	0.001±0.001	0.0175	0.0163	0.0180	0.0190
7. H. squamipinna	0.1314	0.1516	0.1394	0.1288	0.1482	0.1374	0.004±0.002	0.0124	0.0168	0.0158
8. H. parra	0.1565	0.1425	0.1253	0.1178	0.1342	0.1221	0.0846	0.001±0.001	0.0169	0.0145
9. H. steindachneri	0.1554	0.1483	0.1259	0.1041	0.1157	0.1381	0.1306	0.1277	0.003±0.001	0.0121
10. H. atlanticus	0.1645	0.1396	0.1150	0.1143	0.1372	0.1498	0.1287	0.1018	0.0746	0.005±0.002

TABLE 2 | Pairwise K2P distances between Brachygenys and Haemulon genetic lineages (below the diagonal) and standard errors (above the diagonal). The numbers in bold type represent the intraspecific K2P genetic distances. + Only one sample available. The species identified by letters correspond to the distribution of the specimens as described in the article.

Species	1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16
1. Brachygenys jessiae	-	0.018	0.017	0.019	0.020	0.017	0.019	0.020	0.017	0.020	0.020	0.021	0.021	0.021	0.018	0.018
2. B. chrysargyrea	0.137	0.003	0.016	0.019	0.018	0.017	0.017	0.019	0.017	0.018	0.018	0.017	0.017	0.017	0.020	0.020
3. B. californiensis	0.139	0.126	0.001	0.016	0.018	0.015	0.016	0.017	0.017	0.017	0.017	0.016	0.016	0.015	0.016	0.016
4. Haemulon aurolineatum A	0.154	0.157	0.127	0.000	0.012	0.012	0.012	0.017	0.016	0.016	0.015	0.016	0.017	0.017	0.015	0.014
5. H. plumieri C	0.170	0.139	0.139	0.083	0.001	0.011	0.010	0.016	0.018	0.017	0.016	0.017	0.017	0.017	0.016	0.017
6. H. plumieri B	0.139	0.139	0.121	0.079	0.064+	0.000	0.006	0.015	0.017	0.017	0.016	0.019	0.019	0.015	0.015	0.015
7. H. plumieri A	0.152	0.134	0.120	0.080	0.048+	0.024+	0.004	0.016	0.017	0.017	0.015	0.018	0.018	0.015	0.016	0.016
8. H. melanurum	0.160	0.160	0.133	0.133	0.127	0.119	0.120	0.001	0.017	0.016	0.018	0.019	0.019	0.015	0.015	0.016
9. H. squamipinna	0.131	0.151	0.139	0.138	0.159	0.143	0.143	0.137	0.003	0.012	0.017	0.016	0.016	0.016	0.016	0.016
10. H. parra	0.156	0.142	0.125	0.129	0.138	0.133	0.132	0.122	0.084	0.001	0.017	0.015	0.015	0.016	0.016	0.016
11. H. steindachneri	0.155	0.148	0.125	0.120	0.124	0.120	0.110	0.138	0.130	0.127	0.002	0.012	0.012	0.015	0.015	0.014
12. H. atlanticus B	0.171	0.139	0.121	0.123	0.127	0.154	0.138	0.151	0.128	0.104	0.073+	0.001	0.004	0.016	0.015	0.015
13. H. atlanticus A	0.162	0.139	0.113	0.131	0.129	0.153	0.136	0.149	0.128	0.101	0.074+	0.012+	0.001	0.016	0.016	0.016
14. H. aurolineatum B	0.185	0.143	0.120	0.138+	0.135	0.116	0.122	0.110	0.133	0.118	0.114	0.127	0.129	-	0.014	0.014
15. H. aurolineatum C	0.151	0.158	0.119	0.116+	0.120	0.109	0.119	0.105	0.131	0.122	0.107	0.118	0.122	0.098+	0.002	0.005
16. H. aurolineatum D	0.149	0.165	0.117	0.108+	0.125	0.112	0.122	0.111	0.127	0.116	0.102	0.112	0.112	0.106+	0.018+	0.003

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Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br

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Molecular identification of Brachygenys and Haemulon species (Perciformes: Haemulidae) from the Brazilian coast

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[1] Edited-by

Fernando Gibran