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A Review of the Mitogenomic Phylogeny of the Chondrichthyes

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Divino Bruno da Cunha, Luis Fernando da Silva Rodrigues‐Filho and João Bráullio de Luna Sales

Submitted: 01 February 2017 Reviewed: 06 June 2017 Published: 20 December 2017

DOI: 10.5772/intechopen.70028

From the Edited Volume

Chondrichthyes - Multidisciplinary Approach

Edited by Luis Fernando da Silva Rodrigues Filho and João Bráullio de Luna Sales

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Abstract

The phylogenetic analysis of the Chondrichthyes has been the subject of intense debate over the past two decades. The principal relationships within the group based on the analysis of morphological traits are inconsistent with the available molecular topologies, and the phylogeny of these animals is highly controversial, at all levels, ranging from superorders to families and even the genera within families. With the recent development of new generation sequencing (NGS), many phylogenies are now being inferred based on the complete genome of the species. In 2015 and 2016 alone, around 21 new elasmobranch genomes were made available in GenBank. In this context, the principal objective of the present study was to infer the phylogeny of the sharks and rays based on the complete mitochondrial genomes available in the literature. A total of 73 mitogenomes of chondrichthyan species were analyzed. The phylogenetic trees generated rejected the “Hypnosqualea” hypothesis and confirmed the monophyly of the Neoselachii and Batoidea as sister groups of the sharks. These mitogenomic analyses provided ampler and more complete insights into the relationships between the sharks and rays, in particular, the topologies obtained by the analyses revealed a number of incongruities in certain groups of sharks and rays, and the interrelationships between them.

Keywords

  • phylogeny
  • Chondrichthyes
  • mitogenomic
  • sharks and rays

1. Introduction

The Chondrichthyes (sharks, rays, and chimeras) are a diverse group of animals that occupy a key position in the phylogeny of the vertebrates, as one of their most ancient lineages [1, 2]. Estimates of the diversification of the group based on DNA sequences are of the order of 300–460 million years ago. The class Chondrichthyes currently includes 14 orders and 60 families with approximately 1200 species [35]. The group of chondrichthyans with the greatest species diversity is the Batoidea (approximately 494 species), followed by the sharks, with around 500 species [4, 5]. The systematics of the Chondrichthyes have been the subject of considerable debate over the past two decades, and the phylogeny of these animals is still controversial, at all levels, ranging from superorders to families and even the genera within families [6].

Most of the hypotheses on the phylogenetic relationships among chondrichthyan species are based on morphological traits, in particular, the “Hypnosqualea” hypothesis [7, 8], which proposes that the batoids are derived sharks related intimately to the sawfish and angel sharks. However, most molecular phylogenies have rejected the “Hypnosqualea” hypothesis emphatically [3, 911].

A large number of morphological hypotheses have also been proposed to account for the arrangement of the shark orders, such as Ref. [12], which grouped the Squalomorphii and Squatinomorphii together, based on the synapomorphic nature of the orthostatic suspension of the maxilla within the ocular orbit, with the sharks of this clade being referred to as the “orthopedic” forms. In the case of the Galeomorphii and Squalimorphii, a number of studies, both molecular and morphological, have revealed a variety of controversial relationships within each group, and even the relationships among the orders vary between studies. One major example is the position of the Heterodontiformes, which has yet to be resolved [3, 7, 9, 10, 13, 14].

One other unresolved question is the phylogenetic position of the orders within the Galeomorphii, in which the available morphological inferences place Lamniformes as the sister order of the Carcharhiniformes [7, 15], although molecular studies have confirmed that the Orectolobiformes is the sister group of the Carcharhiniformes [13]. The topologies generated in other studies have nevertheless placed Lamniformes as the sister order of the Carcharhiniformes. On a more basal taxonomic level, there is even less agreement among the studies, and the taxonomic status of many Carcharhiniformes families is still unclear, such as the paraphyletism of the hammerhead sharks (Sphyrna) [14, 16, 17].

Another important question is the evidence of extensive paraphyly between the families of the Carcharhiniformes. Winchell et al. [18] concluded that the Scyliorhinidae is paraphyletic, a hypothesis confirmed by Refs. [12, 19]. Based on nuclear and mitochondrial sequences, these authors also proposed that the family Triakidae is paraphyletic, an arrangement confirmed by Ref. [20] based on a number of mitochondrial markers and the nuclear RAG1 gene, which contradicts the hypothesis of monophyly for the Triakidae. Similarly, the relationships among the members of the Batoidea remain unclear [15, 2123]. In general, for example, four groups are recognized, the stingrays (Myliobatiformes), electric rays (Torpediniformes), sawfish (Pristiformes), skates, and guitarfish (Rajiformes), although the relationships among these groups are still undefined [2125]. In addition, a number of new species of ray have been described recently, and the radiation patterns of this group have been better identified [2529].

The most recent molecular analyzed the complete mitochondrial genomes of 48 elasmobranch species, and rejected the “Hypnosqualea” hypothesis. The authors of this study recuperated the monophyly of the Lamnidae, with the families arranged as (Mitsukurinidae (Alopiidae, Megachasmidae) (Odontaspididae (Cetorhinidae (Lamnidae))) [6]. It is important to note that most chondrichthyan topologies are based on DNA sequences from only a few markers, such as a single nuclear or mitochondrial gene, or a combination of these two genes, and the sequences rarely exceed a length of 6 kb [3, 911], except for Ref. [6]. More recently, however, improvements in the speed and accuracy of new generation sequencing (NGS), and the reduction of laboratory costs, have provided a large number of molecular markers, amplifying considerably the analytical perspectives in the fields of phylogenetic and phylogenetic research, and the potential for the study of molecular ecology in a wide range of organisms [3032]. In 2015 and 2016 alone, around 21 new elasmobranch genomes were made available in GenBank.

Mitochondrial markers are widely used in phylogenetic analyses in a diversity of organisms due to the relatively simple sequencing procedures and the high rates of nucleotide substitution [33]. However, the analysis of the complete mtDNA genome may provide a much richer source of genetic information for phylogenetic inferences in comparison with the more traditional approach, based on the analysis of single or multiple genes [32]. In this context, the principal objective of the present study was to provide phylogenetic inferences on the Chondrichthyes based on the complete mitochondrial genome, and a more comprehensive understanding of the relationships among the species of sharks and rays.

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2. Materials and methods

All 73 mitogenomes analyzed in the present study were obtained from the GenBank public database (Table 1). The sequences were aligned automatically by Clustal and colleagues [34], run in the BioEdit sequence editor [35], which was used for visual inspection and possible corrections. The phylogenetic trees were rooted with the species Callorhincus milli and Chimaera monstrosa, which are considered to be most closely related to the sharks and rays, based on the results of previous studies [3, 10, 11]. The Bayesian inference was run in Mr. Bayes 3.0b4 [36], using the GTR + I + G model, which was selected by jModelTest 2 [37], based on the Bayesian information criterion (BIC) [38]. A Metropolis‐coupled Markov chain Monte Carlo (MCMCMC) was executed with four chains run for 100,000,000 generations, using the default parameters. The quality of the run was verified in Tracer v1.6 [39]. The maximum likelihood tree was generated in PhyML 3.0 [40], using the GTR + I + G model, selected by jModelTest 2 [37], based on the Akaike information criterion (AIC), with the confidence interval being established by a bootstrap of 1000 replicates [41]. All the trees were visualized and edited in FigTree v.1.4.3 [42]. The distances among the taxa were calculated using NeighborNet, run in SplitsTree [43].

Order/speciesFamilyGenBank
Carcharhiniformes
Carcharhinus leucas_G1CarcharhinidaeNC023522
Carcharhinus leucasCarcharhinidaeKJ210595
Carcharhinus maclotiCarcharhinidaeNC024862
Carcharhinus sorrahCarcharhinidaeNC024055
Carcharhinus acronotusCarcharhinidaeNC024596
Carcharhinus plumbeusCarcharhinidaeKF801102
Carcharhinus falciformisCarcharhinidaeKF801102
Carcharhinus obscurusCarcharhinidaeNC020611
Carcharhinus melanopterusCarcharhinidaeNC024284
Carcharhinus amblyrhyncoidesCarcharhinidaeNC023948
Carcharhinus longimanusCarcharhinidaeKM434158.1
Carcharhinus brevipinnaCarcharhinidaeKM244770.1
Triaenodon obesusCarcharhinidaeKJ748376.1
Prionace glaucaCarcharhinidaeNC022819
Glyphis garrickiCarcharhinidaeNC023361
Glyphis glyphisCarcharhinidaeKF006312
Galeocerdo cuvier cuvierCarcharhinidaeNC022193
Scoliodon macrorhynchosCarcharhinidaeJQ693102
Sphyrna zygaenaSphyrnidaeKM489157
Sphyrna lewiniSphyrnidaeNC022679
Sphyrna tiburoSphyrnidaeKM453976
Eusphyra blochiiSphyrnidaeKU892590.1
Mustelus griseusTriakidaeNC023527
Mustelus manazoTriakidaeNC000890
Scyliorhinus caniculaScyliorhinidaeNC022415
Lamniformes
Carcharodon carchariasLamnidaeNC022691
Lamna ditropisLamnidaeNC024269
Isurus oxyrinchusLamnidaeNC022691
Isurus paucusLamnidaeNC024101
Cetorhinus maximusCetorhinidaeNC024101
Carcharias taurusOdontaspididaeNC023266
Alopias pelagicusAlopiidaeNC023520
Alopias superciliosusAlopiidaeNC021443
Megachasma pelagiosMegachasmidaeNC021442
Mitsukurina owstoniMegachasmidaeNC011825
Orectolobiformes
Orectolobus japonicusOrectolobidaeKF111729
Rhyncodon typusRhincodontidaeNC023455
Chiloscyllium griseumHemiscylliidaeNC017882
Chiloscyllium plagiosumHemiscylliidaeNC012570
Chiloscyllium punctatumHemiscylliidaeNC016686
Stegostoma fasciatumStegostomatidaeKU057952.1
Heterodontiformes
Heterodontus francisciHeterodontidaeNC003137
Heterodontus zebraHeterodontidaeNC021615
Squatiniformes
Squatina formosaSquatinidaeNC025328
Squatina japonicaSquatinidaeNC024276
Squatina nebulosaSquatinidaeNC025578
Squatina formosaSquatinidaeNC025328
Squaliformes
Squalus acanthiasSqualidaeNC002012
Cirrhigaleus australisSomniosidaeKJ128289
Squaliolus aliaeDalatiidaeKU873080.1
Somniosus pacificusSomniosidaeNC022734
Pristiophoriformes
Pristiophorus japonicusPristiophoridaeNC_024102
Hexanchiformes
Hexanchus griseusHexanchidaeKF894491
Myliobatiformes
Gymnura poeciluraGymnuridaeNC_024102
Dasyatis akajeiDasyatidaeNC021132.1
Torpediformes
Narcine entemedorNarcinidaeKM386678
Rajiformes
Rhinobatos schlegeliiRhinobatidaeNC023951
Rhinobatos hynnicephalusRhinobatidaeNC022841
Rhina ancylostomaRhinobatidaeKU721837.1
Zearaja chilensisRajidaeKJ913073
Hongeo koreanaRajidaeNC021963
Dipturus kwangtungensisRajidaeNC023505
Raja pulchraRajidaeNC025498
Raja rhinaRajidaeKC914434
Okamejei hollandiRajidaeKP756687
Okamejei kenojeiRajidaeNC007173
Atlantoraja castelnauiArhynchobatidaeNC025942
Pavoraja nitidaArhynchobatidaeNC024599
Pristiformes
Anoxypristis cuspidataPristidaeNC026307
Pristis clavataPristidaeKF381507
Pristis pectinataPristidaeNC027182
Chimaeriformes
Callorhinchus milliCallorhinchidaeNC014285
Chimaera monstrosaChimaeridaeAJ310140

Table 1.

Complete mitochondrial genome of the elasmobranch species analyzed in the present study.

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3. Results and discussion of the phylogenetic relationships

The phylogenetic analyses of the 73 shark and ray mitogenomes supports a basic division into four major groups, the Galeomorphii, Squalomorphii, Squatinomorphii, and Batoidea (Figure 1), as suggested in previous molecular studies, based on both mitochondrial and nuclear genes [3, 6, 911, 13]. The Bayesian and the maximum likelihood phylogenetic trees of the mitochondrial genomes had highly similar topologies, with the Batoidea being placed as the most basal group, sister group to all the others [3, 6, 11, 13]. The results of this analysis reject emphatically the “Hypnosqualea” hypothesis based on morphological data, which proposes that the Batoidea is part of the shark group, and represents a highly derived lineage of this group (see [7, 8, 44]). The molecular and morphological data are highly divergent with regard to this question.

Figure 1.

Bayesian inference and maximum likelihood generated from the complete mitochondrial genome of the Chondrichthyes. Only branches with bootstrap values below 100% are shown.

The phylogenetic reconstruction obtained in the present study confirms the monophyly of the modern sharks (neoselachian), although another controversial question is the existence of the superorders proposed by Ref. [44], based on cladistic analyses of morphological data, which indicated the existence of four superorders—Galeomorphii, Squalomorphii, Squatinomorphii, and Batoidea. While the results of the present study confirm the existence of these four major groups, there are some differences in their arrangement (Figure 1) [6, 9, 11, 13].

The data support the monophyly of the order Squaliformes, with Hexanchus griseus (Hexanchiformes) at the base of the clade, followed by squaliformes as the sister taxon of the Squatiniformes and Pristiophoriformes. An important feature of the arrangement of the species within the Squatiniformes is the position of Squatina nebulosa as sister taxon of S. formosa, with S. japonica in a basal position in the clade. Pristiophorus japonicus is a sister group of this same clade, which highlights the paraphyletism of the two orders (Squatiniforme and Pristiophoriformes), an arrangement proposed by Ref. [13], who were nevertheless unable to define the position of S. nebulosa. The close relationship between the orders Squaliformes and Squatiniformes is consistent with [12], who used the projection of the cartilage of the upper mandible into the ocular orbit as a synapomorphic trait, with the sharks of this clade being denominated “orbitostylic” sharks. This arrangement confirms the findings of previous studies based on molecular markers [3, 6, 13, 18].

In the case of the Galeomorphii, it is important to note that the Heterodontiformes was identified as the most basal taxon of this superorder, in a clade supported by high probability values (Figure 1). The Lamniformes is the sister group of Carcharhinifromes, which is placed as sister group of the Orectolobiformes with strong statistical support. The taxonomic position of the order Heterodontiforme within the Galeomorphii is considered to be extremely controversial [13]. Some studies have identified the Heterodontiformes as the most basal order, with Orectolobiformes being more closely related to the Lamniformes and Carcharhinifromes, a grouping supported by both morphological [7, 8] and molecular studies [3, 6, 9]. However, Ref. [18], using 5.8 kb of nuclear gene sequences (major and minor rRNA subunits), and Ref. [14], who analyzed mitochondrial data, indicated a closer relationship between the Orectolobiformes and Lamniformes [6, 10, 13].

The family‐level phylogenetic inferences within the Carcharhinifromes reinforced the paraphyletism of this order, with the clade of the hammerhead sharks (Sphyrnidae) being placed as a sister group of the sharks (Carcharhinidae). Scyliorhinus canicula (Scyliorhinidae) was the most basal of the Carcharhiniformes, with Mustelus manazo (Triakidae) and Galeocerdo cuvier (Carcharhinidae) being placed close to all the other sharks, with high levels of statistical support (Figure 1). This arrangement is inconsistent with the results of Ref. [6], who used the complete mtDNA genome, and placed Scoliodon macrorhincos as a sister group of the sharks, with the sphyrnas as a sister group of this same clade. However, the arrangement observed here is in agreement with the studies of Refs. [3, 11, 13]. The most likely explanation for the lack of agreement between the results of the present study and those of Ref. [6] may be the difference in the number of species analyzed, given that an additional 24 mitogenomes were included in the present study. In addition, the pairs of species Carcharhinus sorrah/C. macloti, C. amblyrhyncoides/C. leucas, and C. brevipania/Triaenodon obesus/C. acronotus were involved in a polytomy. The polytomic pattern within Carcharhinidae is probably related to the low‐levels of intrinsic genetic variability of sharks (Figure 2) [47]. The results of the present study are consistent with those of other molecular phylogenies [10, 13, 17, 24]. The analyses support the monophyly of the Lamniformes, with high probability values. The genus Lamna is the sister group of Carcharodon and Isurus, the most derived taxa of this group. This arrangement is supported by both the morphological data (Compagno 1990) and molecular inferences [6, 13, 17].

Figure 2.

Genealogy showing the relationships between the orders of Chondrichthyes based on the complete mitochondrial genome of 73 species of sharks and rays. The two black circles on the right represent the out group.

The monophyly of the rays was also supported by high probability values [3, 6, 9, 10, 16]. The analysis revealed the formation of four well‐defined groups—Torpediformes, Rajiformes, Pristiformes, and Myliobatiformes—with branches supported by high bootstrap values (Figure 1). These results are consistent with previous studies based on the analysis of morphological and molecular data [2125]. One other important finding of the present study was the arrangement of the orders Torpediniformes and Rajiformes close to the root of the tree (Figure 2). At the family level, two clades were observed, one containing the Narcinidae (the electric rays) as the most primitive taxon of the group, with the Rajidae (skates) and Arhynchobatidae grouped in the same clade, all on branches with high statistical support. The arrangement of the Narcinidae (Torpediniformes) is inconsistent with the morphological inferences, which assume that Pristiformes is the most basal order of the Batoidea [11, 15, 24]. However, the principal phylogenies based on mitochondrial and nuclear markers indicate that the Rajoidei is the sister group of all the other members of the Batoidea [3, 6, 16, 21, 22].

The second clade includes Zapteryx exasperata (Rhinobatidae) as the most basal taxon, with Rhinobatos hynnicephalus/R. schlegelii as sister taxa. The family Rhinobatidae is placed as a sister group of the Pristidae, which is represented by Anoxpristis cuspidata, Pristis clavata, and P. pectinata, with all branches being supported by high probability values. The Myliobatidae is placed in this same clade as the sister group of the Rhinobatidae, an arrangement with high values in the Bayesian inference, and more moderate ones in the maximum likelihood analysis. The grouping of the sawfish (Pristiformes) with the guitarfish (Rhinobatidae) disagrees with the morphological phylogenies, which identifies the Pristiformes as the most primitive group of the Batoidea [23, 46]. However, this arrangement is supported by other molecular studies (see [3, 6, 16, 21]).

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4. Conclusion

The analyses of the mitochondrial genome provided an ampler and more complete overview of the relationships within the Chondrichthyes, with the topologies highlighting a number of inconsistencies in some of the taxonomic groups of sharks and rays, principally in terms of the interrelationships among groups [13]. It is important to note that the phylogenetic relationships within the genera of these groups are still poorly understood, and that a mitogenomic phylogeny, including a much broader diversity of taxa, may provide more comprehensive insights into the relationships among the species of these organisms. Among other conclusions, the phylogenetic trees rejected the “Hypnosqualea” hypothesis and confirmed the monophyly of the Neoselachii, and Batoidea as the sister group of the sharks [16, 21], in agreement with most of the available molecular phylogenies. The Batoidea is a monophyletic group, in which the Torpediniformes and Rajiformes are the most ancestral orders, contradicting the morphological analyses, which identifies the Pristiformes as the most basal order. The phylogenetic trees supported conclusively the division of the Batoidea into four groups, the Torpediniformes, Rajiformes, Pristiformes, and Myliobatiformes [45].

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Acknowledgments

We would like to thank the Bragança campus of the Federal University of Pará and the Evolution Laboratory. We are also grateful to the Northern Elasmobranchs study group.

References

  1. 1. Renz AJ, Meyer A, Kuraku S. Revealing less derived nature of cartilaginous fish genomes with their evolutionary time scale inferred with nuclear genes. PLoS ONE. 2013;8:e66400. DOI: 10.1371/journal.pone.0066400
  2. 2. Nelson JM. Fishes of the World. New York: Wiley; 1994
  3. 3. Heinicke MP, Naylor GJP, Hedges SB. Cartilaginous fishes (Chondrichthyes). In: Hedges SB, Kumar S, editors. The Timetree of Life. New York: Oxford University Press; 2009. p. 320
  4. 4. Weigmann S. Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. Journal of Fish Biology. 2016;88:837-1037. DOI: 10.1111/jfb.12874
  5. 5. Gemaque R, Monteiro ILP, Gomes F, Sodré D, Sampaio I, Sales JBL, Rodrigues Filho LFS. Why implement measures to conserve the diversity of Elasmobranchs? The case of the northern coast of Brazil. Revista da Biologia. 2017;17:1-6. DOI: 10.7594/revbio.17.02.01
  6. 6. Diaz‐Jaimes P, Uribe‐Alcocer M, Hinojosa‐Alvarez S, Sandoval‐Laurrabaquio N, Adams DH, García De León FJ. The complete mitochondrial DNA of the bull shark (Carcharhinus leucas). Mitochondrial DNA. 2014;27(1):717-8. DOI: 10.3109/19401736.2014.913157
  7. 7. de Carvalho MR, Maisey JG. Phylogenetic relationships of the late jurassic shark protospinax Woodward 1919 (Chondrichthyes: Elasmobranchii). In: Arratia G, Viohl G, editors. Mesozoic Fishes: Systematics and Paleoecology. Munich: Verlag Dr Friedrich Pfeil; 1996. pp. 9-46
  8. 8. Shirai S: Phylogenetic interrelationships of neoselachians (Chondrichthyes: Euselachii). In: Stiassny MLJ, Parenti LR, Johnson GD, editors. Interrelationships of Fishes. San Diego: Academic Press; 1996. pp. 9-34
  9. 9. Naylor GJP, Ryburn JA, Fedrigo O, López JA. Phylogenetic relationships among the major lineages of modern elasmobranchs. In: Hamlett WC, Jamieson BGM, editors. Reproductive Biology and Phylogeny 3. Science Publishers; 2005. pp. 1-25
  10. 10. Human BA, Owen EP, Compagno LJV, Harley EH. Testing morphologically based phylogenetic theories within the cartilaginous fishes with molecular data, with special reference to the catshark family (Chondrichthyes; Scyliorhinidae) and the interrelationships within them. Molecular Phylogenetics and Evolution. 2006;39:384-391
  11. 11. Gkafas GA, Megalofonou P, Batzakas G, Apostolidis AP, Exadactylos A. Molecular phylogenetic convergence within Elasmobranchii revealed by cytochrome oxidase subunits. Biochemical Systematics and Ecology. 2015;61:510-515. DOI: 10.1016/j.bse.2015.07.025
  12. 12. Maisey JG. Higher elasmobranch phylogeny and biostratigraphy. Zoological Journal of the Linnean Society. 1984;82:33-54
  13. 13. Vélez‐Zuazo X, Agnarsson I. Shark tales: A molecular species‐level phylogeny of sharks (Selachimorpha, Chondrichthyes. Molecular Phylogenetics and Evolution. 2011;58:207-217
  14. 14. Douady CJ, Dosay M, Shivji MS, Stanhope MJ. Molecular phylogenetic evidence refuting the hypothesis of Batoidea (rays and skates) as derived sharks. Molecular Phylogenetics and Evolution. 2003;26:215-221
  15. 15. Compagno LJV. Interrelationships of living elasmobranchs. Zoological Journal of the Linnean Society. 1973;53:15-61
  16. 16. Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR. A sequence based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bulletin of the American Museum of Natural History. 2012;367:1-262
  17. 17. Lim DD, Motta P, Mara K, Martin AP. Phylogeny of hammerhead sharks (family Sphyrnidae) inferred from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution. 2010;55:572-579
  18. 18. Winchell CJ, Martin AP, Mallatt J. Phylogeny of elasmobranchs based on LSU and SSU ribosomal RNA genes. Molecular Phylogenetics and Evolution. 2004;31:214-224
  19. 19. Iglésias SP, Lecointre G, Sellos DY. Extensive paraphylies within sharks of the order Carcharhiniformes inferred from nuclear and mitochondrial genes. Molecular Phylogenetic Evolution. 2005;34:569-583
  20. 20. Lopez JA, Ryburn JA, Fedrigo O, Naylor GJ. Phylogeny of sharks of the family Triakidae (Carcharhiniformes) and its implications for the evolution of carcharhiniform placental viviparity. Molecular Phylogenetic Evolution. 2006;40:5060
  21. 21. Aschliman NC, Nishida M, Miya M, Inoue JG, Rosana KM, Naylor GJP. Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Molecular Phylogenetics and Evolution. 2012;63:28-42. DOI: 10.1016/j.ympev.2011.12.012
  22. 22. Pavan‐Kumar A, Gireesh‐Babu P, Babu PP, Jaiswar AK, Hari Krishna V, Prasasd KP. Molecular phylogeny of elasmobranchs inferred from mitochondrial and nuclear markers. Molecular Biology Reports. 2013;41:447-457. DOI: 10.1007/s11033‐013‐2879‐6
  23. 23. McEachran JD, Aschliman N. Phylogeny of batoidea. In: Carrier JC, Musick JA, Heithaus MR, editors. Biology of Sharks and Their Relatives. Boca Raton, FL: CRC Press; 2004. pp. 79-113
  24. 24. Nishida K. Phylogeny of the suborder Myliobatoidei. Mem. Fac. Fish Hokkaido Univ. 1990;37:1-108
  25. 25. Naylor GJP, Caira JN, Jensen K, Rosana KAM, Straube N, Lakner C. Elasmobranch phylogeny: A mitochondrial estimate based on 595 species. In: Carrier JC, Musick JA, Heithaus MR, editors. Biology of Sharks and Their Relatives. 2nd ed. Boca Raton: CRC Press; 2012. pp. 31-56
  26. 26. Last PR, Naylor GJP, Manjaji‐Matsumoto M. A revised classification of the family Dasyatidae (Chondrychthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa. 2016;4139:345-368
  27. 27. Last PR, Henderson AC, Naylor GJP. Acroteriobatus omanesis (Batoidea: Rhinobatidae), a new guitarfish from the Gulf of Oman. Zootaxa. 2016;4144:276-286
  28. 28. Last PR, Kyne PM, Compagno LJV. A new species of wedgefish Rhynchobatus cooki (Rhinopristiformes, Rhinidae) from the Indo‐West Pacific. Zootaxa. 2016;4139:233-247
  29. 29. Puckridge M, Last PR, White WT, Andreakis N. Phylogeography of the indo‐west pacific maskrays (Dasyatis, Neotrygon): A complex example of chondrichthyan radiation in the Cenozoic. Ecology and Evolution. 2013;3:217-232
  30. 30. Avise JC. Molecular Markers, Natural History and Evolution. Sunderland MA: Chapman Hall; 1994. p. 511
  31. 31. Templeton AR. The role of molecular genetics in speciation studies. In: Schierwater B, Streit B, Wagner GP, editors. Molecular Ecology and Evolution: Approaches and Applications. Basel: Birkhäuser Verlag; 1994. pp. 455-475
  32. 32. Qin J, Zhang Y, Zhou X, Kong X, Wei S, Ward RD, Zhang A. Mitochondrial phylogenomics and genetic relationships of closely related pine moth (Lasiocampidae: Dendrolimus) species in China, using whole mitochondrial genomes. BMC Genomics. 2015;16:428-439
  33. 33. Boore JL. Animal mitochondrial genomes. Nucleic Acids Research. 1999;27:1767-1780
  34. 34. Thompson JD, Higgins DG, Gibson TJ, Clustal W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position‐specific gap penalties and weight matrix choice. Nucleic Acids Research. 1994;22:4673-4680
  35. 35. Hall TA. BioEdit: A user‐friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999;41:95-98
  36. 36. Ronquist F, Huelsenbeck JP. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572-1574
  37. 37. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nature Methods. 2012;9:772-772
  38. 38. Posada D, Buckley TR. Model selection and model averaging in phylogenetics: Advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Systematic Biology. 2004;53:793-808
  39. 39. Rambaut A, Drummond AJ. Tracer version 1.5 [computer program] [Internet]. 2009. Available from: http://beast.bio.ed.ac.uk
  40. 40. Guindon S, Dufayard J‐F, Lefort V, Anisimova M, Hordijk W. New algorithms and methods to estimate maximum‐likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology. 2010;59:307-321
  41. 41. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39:783-791
  42. 42. Rambaut A. FigTree v1.4 [Internet]. 2013. Available from: http://tree.bio.ed.ac.uk/software/figtree/
  43. 43. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution. 2006;23:254-267
  44. 44. Compagno LJV. Phylogenetic relationships of living sharks and rays. American Zoologist. 1977;17:303-322
  45. 45. White WT, Naylor GJP. Resurrection of the family Aetobatidae (Myliobatiformes) for the pelagic eagle rays, genus Aetobatus. Zootaxa. 2016;4139:435-438
  46. 46. McEachran JD, Dunn KA, Miyake T. Interrelationships within the batoid fishes (Chondrichthyes: Batoidea). In: Stiassney MLJ, Parenti LR, Johnson GD, editors. Interrelationship of Fishes. New York: Academic Press; 1996. pp. 63-84
  47. 47. Rodrigues‐Filho LFS, Rocha TC, Rêgo PS, Schneider H, Sampaio I, Vallinoto M. Identification and phylogenetic inferences on stocks of sharks affected by the fishing industry off the Northern coast of Brazil. Genetics and Molecular Biology. 2009;32:405-413

Written By

Divino Bruno da Cunha, Luis Fernando da Silva Rodrigues‐Filho and João Bráullio de Luna Sales

Submitted: 01 February 2017 Reviewed: 06 June 2017 Published: 20 December 2017