Systematics of the grey mullets (Teleostei: Mugiliformes: Mugilidae): Molecular phylogenetic evidence challenges two centuries of morphology-based taxonomy

https://doi.org/10.1016/j.ympev.2012.03.006Get rights and content

Abstract

The family Mugilidae comprises mainly coastal marine species that are widely distributed in all tropical, subtropical and temperate seas. Mugilid species are generally considered to be ecologically important and they are a major food resource for human populations in certain parts of the world. The taxonomy and systematics of the Mugilidae are still much debated and based primarily on morphological characters. In this study, we provide the first comprehensive molecular systematic account of the Mugilidae using phylogenetic analyses of nucleotide sequence variation at three mitochondrial loci (16S rRNA, cytochrome oxidase I, and cytochrome b) for 257 individuals from 55 currently recognized species. The study covers all 20 mugilid genera currently recognized as being valid. The family comprises seven major lineages that radiated early on from the ancestor to all current forms. All genera that were represented by two species or more, except Cestraeus, turned out to be paraphyletic or polyphyletic. Thus, the present phylogenetic results generally disagree with the current taxonomy at the genus level and imply that the anatomical characters used for the systematics of the Mugilidae may be poorly informative phylogenetically. The present results should provide a sound basis for a taxonomic revision of the mugilid genera. A proportion of the species with large distribution ranges (including Moolgarda seheli, Mugil cephalus and M. curema) appear to consist of cryptic species, thus warranting further taxonomic and genetic work at the infra-generic level.

Highlight

► The phylogeny of the Mugilidae family was inferred from mitochondrial DNA sequences. ► The family comprises seven major lineages that radiated early from the ancestor to all current Mugilidae. ► All genera represented by two species or more except Cestraeus, turned out to be paraphyletic or polyphyletic. ► Several species with wide geographic distribution, including the cosmopolitan Mugil cephalus, comprise cryptic species.

Introduction

The Mugilidae (or grey mullets) is a speciose family of Teleostean fishes, which has representatives in various coastal aquatic habitats of the world’s tropical, subtropical and temperate regions (Thomson, 1966). Despite the ecological and economical importance of grey mullet (Thomson, 1966), the taxonomy and evolutionary relationships among the species so far remains largely unresolved (Harrison et al., 2007). A major reason is that most morphological characters classically used in species identification and/or systematics are remarkably similar within the family (Schultz, 1946, Thomson, 1997). Thus, it has been a challenging task to define species and genera and, during the last 130 years, up to 281 nominal species and 45 nominal genera have been proposed for the Mugilidae (Thomson, 1997, Eschmeyer and Fricke, 2011). The number of mugilid species has probably been overestimated since most of the earlier taxonomic work relied on the examination of specimens collected locally, without comparing these specimens to morphologically similar species described elsewhere (Thomson, 1954).

The first thorough taxonomic revision of the Mugilidae was produced by Schultz (1946), who mainly used mouth anatomy to define both genera and species. Schultz (1946) validated only ten previously defined mugilid genera and described three new ones, a revision that was subsequently questioned (see review in Ghasemzadeh et al. (2004)). Mugilid taxonomy and nomenclature have still not been finalized (Harrison et al., 2007), with between 14 and 20 genera being recognized as valid according to the most recent revisions (Thomson, 1997, Ghasemzadeh, 1998, Nelson, 2006). The Integrated Taxonomic Information System recognizes 16 valid genera (http://www.itis.gov/; information retrieved on 16 August 2011), while Eschmeyer and Fricke (2011) list 20 valid genera. Two genera, Liza and Mugil, currently represent 40% of the species richness within the family Mugilidae (Eschmeyer and Fricke, 2011). The other genera consist of fewer species and 40% (8/20) are monotypic (Eschmeyer and Fricke, 2011). The high proportion of monotypic genera may reflect the general difficulty in classifying mugilid species on the basis of the few diagnostic or synapomorphic characters that have been considered so far. Alternatively, this may indicate an ancestral radiation event followed by a long period of stasis.

Anatomical differences among mugilid species are not easily interpretable from a cladistic perspective, as shown by the conflicting morpho-anatomical phylogenetic hypotheses proposed by different authors (Fig. 1A–E). For example, Rhinomugil, which was considered by Schultz (1946) as an aberrant genus and was tentatively placed by him at an intermediate position in the mugilid tree (Fig. 1A), was later assessed to be closely related to the genus Liza and other reportedly recently derived mugilid genera (Thomson, 1997, Ghasemzadeh, 1998). Similarly, Harrison and Howes (1991) and some other authors (Fig. 1C–E) have suggested that the rudimentary pharyngobranchial organ in Cestraeus is a plesiomorphic character. In contrast, Schultz (1946) regarded Cestraeus to be a recently derived genus, pointing its highly specialized lips and teeth as supporting evidence (assumed by him to be an apomorphic anatomical feature in the Mugilidae). Thomson (1997) used both internal (intestine, stomach, pyloric caeca) and external (nostrils, teeth, scales, lips, preorbital bones, jaw) anatomical structures to resolve the polytomies remaining in the phylogeny proposed by Harrison and Howes (1991) (Fig. 1C). Thomson (1997) suggested that the genera Chelon, Liza and Oedalechilus are closely related (Fig. 1D). These three genera had been synonymized by Schultz (1946), but Harrison and Howes (1991) had assigned them distinct lineages (Fig. 1C) due to divergent views on how to weigh the anatomical characters.

In the last decade, molecular studies have provided many insights into the systematics of fishes at all taxonomic levels (Chen and Mayden, 2010) while phylogeographic studies have provided important insight into evolutionary forces that shape intraspecific genetic diversity (Avise, 2000). The Mugilidae were initially placed in an intermediate position in the Acanthomorph tree because of putatively plesiomorphic morphological features shared with Atherinomorpha, themselves considered as more basal Teleosteans (Stiassny, 1993). The Mugilidae are actually related to other advanced teleosts within the Percomorpha (Chen et al., 2003, Chen et al., 2007, Mabuchi et al., 2007, Miya et al., 2003). The placement of the Mugilidae in the Acanthomorph tree has been further explored by Smith and Wheeler, 2006, Smith and Craig, 2007, Setiamarga et al., 2008, and Li et al. (2009).

Phylogenetic relationships within the Mugilidae have largely been based on specimens collected within particular geographic regions, such as India (Menezes et al., 1992), East Asia (Lee et al., 1995, Liu et al., 2010), America (Fraga et al., 2007), and the Mediterranean (Autem and Bonhomme, 1980, Blel et al., 2008, Caldara et al., 1996, Erguden et al., 2010, Gornung et al., 2007, Imsiridou et al., 2007, Murgia et al., 2002, Papasotiropoulos et al., 2001, Papasotiropoulos et al., 2002, Papasotiropoulos et al., 2007, Rossi et al., 1998a, Rossi et al., 2004, Semina et al., 2007, Turan et al., 2005). The above studies have generally demonstrated an early rapid divergence for the Mugil lineage and have led to a questioning of the monophyly of the genera Chelon and Liza (Aurelle et al., 2008). Phylogeographic studies within the Mugilidae have mainly focused on two species of the genus Mugil, namely M. cephalus (Crosetti et al., 1993, Crosetti et al., 1994, Heras et al., 2009, Jamandre et al., 2009, Ke et al., 2009, Liu et al., 2009, Livi et al., 2011, Rocha-Olivares et al., 2000, Rossi et al., 1998b, Shen et al., 2011) and M. curema (Fraga et al., 2007, Heras et al., 2006, Heras et al., 2009). In the process, multiple independent lineages have been uncovered within both M. cephalus and M. curema (Aurelle et al., 2008, Fraga et al., 2007, Heras et al., 2009). Based on the above findings, additional efforts are certainly required to resolve the evolutionary relationships within the Mugilidae at both the generic and species levels.

In this study, the phylogenetic relationships within the Mugilidae were investigated based on the analysis of DNA sequence variations from three mitochondrial loci (16S, COI, and cytb) and using representative taxonomic sampling in order to provide the first comprehensive insight into the systematics of the family. Using the COI gene polymorphism as a marker, Zemlak et al. (2009) have inferred that up to 60% of inshore fish species with an Indo-Pacific distribution might well consist of sibling species. To further address the issue of cryptic species within widely distributed mugilid species, emphasis was placed on geographical sampling of a number of species with large geographic distributions, namely Chelon macrolepis, Crenimugil crenilabis, Moolgarda cunnesius, M. seheli, Mugil cephalus, M. curema and Valamugil buchanani.

Section snippets

Data collection and analysis

It was essential to use a broad taxonomic sampling in order to best represent the phylogenetic diversity within the family Mugilidae (Hillis, 1998) and to provide the most accurate insights into relationships between genera. The many uncertainties concerning the validation of some genera or species required sampling of multiple representatives of each genus, and/or species when possible. Nineteen of the 20 mugilid genera currently recognized as valid (Eschmeyer and Fricke, 2011) were sampled,

Characteristics of the sequence data

Matrix 1 consisted of the full sequences of the amplified fragments of three mitochondrial genes of 46 mugilid individuals and three outgroups, aligned over 3777 bp. The length of the nucleotide sequence of the 16S gene ranged from 1315 to 1355 bp depending on the individual. Indels were therefore required to align sequences. No indel was present in the aligned COI sequences (1405 bp) and cytb sequences (1045 bp). Of the 3777 nucleotides sites, 1834 were variable and 1534 of the latter were

Phylogenetic relationships among Mugilidae genera

The genus rather than the species is currently designated as the analytical unit for a wide range of large-scale analyses in systematics, biogeography and conservation biology (Mandelik et al., 2007, Villaseñor et al., 2005). Consequently, the significance of our results relating to the systematics of the Mugilidae is discussed at the genus level.

Previous investigations using various anatomical characters, have provided conflicting hypotheses on the systematic relationships within the family

Acknowledgments

We thank the numerous people who contributed mugilid samples for this study, namely H. Ashanti, Z. Batang, P. Bearez, A. Bentley, Y. Bettarel, J. Boubee, D.J. Bray, R. Causse, S. Chow, K.W. Conway, P. Cowley, M.T. Craig, I. de Buron, B. Delling, P. Durville, I. Faye, M. Gomon, B. Gourène, A. Graham, C.-C. Hsu, N. Hubert, S. Kleinertz (SPICE II project), B. Kreiser, S. Kullander, S. Lamberth, P. Laleye, H.K. Larson, R. Lessa, M. Louis, H. Masski, R. Mayden, M. McGrouther, M. Mwale, X.-P. Nie, H.

References (84)

  • M.R. Menezes et al.

    Interspecific genetic divergence in grey mullets from the Goa region

    Aquaculture

    (1992)
  • M. Miya et al.

    Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences

    Mol. Phylogenet. Evol.

    (2003)
  • D.H.E. Setiamarga et al.

    Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences

    Mol. Phylogenet. Evol.

    (2008)
  • D. Aurelle et al.

    Molecular phylogeny of Mugilidae (Teleostei: Perciformes)

    Open Mar. Biol. J.

    (2008)
  • J.C. Avise

    Phylogeography: The History and Formation of Species

    (2000)
  • H. Blel et al.

    Phylogenetic relationships in grey mullets (Mugilidae) in a Tunisian lagoon

    Aquaculture Res.

    (2008)
  • J.C. Briggs

    Fishes of worldwide (circumtropical) distribution

    Copeia

    (1960)
  • W.-J. Chen et al.

    A phylogenomic perspective on the new era of ichthyology

    BioScience

    (2010)
  • W.-J. Chen et al.

    Relationships among four genera of mojarras (Teleostei: Perciformes: Gerreidae) from the western Atlantic and their tentative placement among percomorph fishes

    J. Fish Biol.

    (2007)
  • D. Crosetti et al.

    Pronounced genetic structure of mitochondrial DNA among populations of the circumglobally distributed grey mullet (Mugil cephalus Linnaeus)

    J. Fish Biol.

    (1994)
  • R.C. Edgar

    MUSCLE: multiple sequence alignment with high accuracy and high throughput

    Nucl. Acids Res.

    (2004)
  • D. Erguden et al.

    Genetic identification and taxonomic relationship of Mediterranean mugilid species based on mitochondrial 16S rDNA sequence data

    J. Anim. Vet. Adv.

    (2010)
  • Eschmeyer, W.N., Fricke, R. (Eds.), 2011. Catalog of Fishes, Electronic Version....
  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • E. Fraga et al.

    Molecular phylogenetic analyses of mullets (Mugilidae, Mugiliformes) based on two mitochondrial genes

    J. Appl. Ichthyol.

    (2007)
  • Ghasemzadeh, J., 1998. Phylogeny and Systematics of Indo-Pacific mullets (Teleostei: Mugilidae) with Special Reference...
  • J. Ghasemzadeh et al.

    Historical overview of mugilid systematics, with descriptions of Paramugil (Teleostei: Mugiliformes: Mugilidae), new genus. Aqua

    J. Ichthyol. Aquat. Biol.

    (2004)
  • N. Goldman

    Statistical tests of models of DNA substitution

    J. Mol. Evol.

    (1993)
  • E. Gornung et al.

    5S ribosomal RNA genes in six species of Mediterranean grey mullets: genomic organization and phylogenetic inference

    Genome

    (2007)
  • T.A. Hall

    BioEdit: a user-friendly biological sequence alignement editor and analysis program for windows 95/98/NT

    Nucl. Acids Symp. Ser.

    (1999)
  • I.J. Harrison et al.

    The pharyngobranchial organ of mugilid fishes; its structure, variability, ontogeny, possible fonction and taxonomic utility

    Bull. Brit. Mus. Nat. Hist. Zool.

    (1991)
  • Harrison, I.J., Senou, H., 1999. Mugilidae. In: Carpenter, K.E., Niem, V.H. (Eds.), FAO Species Identification Guide...
  • I.J. Harrison et al.

    A new species of mullet (Teleostei: Mugilidae) from Venezuela, with a discussion on the taxonomy of Mugil gaimardianus

    J. Fish Biol.

    (2007)
  • W. Hennig

    Phylogenetic Systematics

    (1966)
  • S. Heras et al.

    Molecular phylogeny of Mugilidae fishes revised

    Rev. Fish Biol. Fish.

    (2009)
  • D.M. Hillis

    Inferring complex phylogenies

    Nature

    (1996)
  • D.M. Hillis

    Taxonomic sampling, phylogenetic accuracy, and investigator bias

    Syst. Biol.

    (1998)
  • J.P. Huelsenbeck et al.

    MrBayes. Bayesian inference of phylogeny

    Bioinformatics

    (2001)
  • A. Imsiridou et al.

    Genetic identification and phylogenetic inferences in different Mugilidae species using 5S rDNA markers

    Aquaculture Res.

    (2007)
  • B.W. Jamandre et al.

    Phylogeography of the flathead mullet Mugil cephalus in the Northwest Pacific inferred from the mtDNA control region

    J. Fish Biol.

    (2009)
  • H.M. Ke et al.

    Genetic diversity and differentiation of grey mullet (Mugil cephalus) in the coastal waters of Taiwan

    Zool. Sci.

    (2009)
  • A.G. Kluge

    A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes)

    Syst. Zool.

    (1989)
  • Cited by (0)

    View full text