New nuclear markers and exploration of the relationships among Serraniformes (Acanthomorpha, Teleostei): The importance of working at multiple scales
Graphical abstract
Highlights
► We explore the relationships within Serraniformes with several specimens per family. ► Based on seven nuclear markers, one never used before: MLL2. ► Several sub-orders and families are not monophyletic. ► Morphological characters are provided for reliable clades in Scorpaenidae.
Introduction
Through molecular phylogenetics studies, the last 15 years provided many surprises for the phylogeny of Percomorpha, the “bush at the top” of Teleosts (Nelson, 1989). Few before would have dared to propose relationships such as for instance the one uniting saithe and cods with john dorys (Wiley et al., 2000, Chen et al., 2003), or a group uniting groupers (Serranidae), perches (Percidae), sticklebacks (Gasterosteidae), searobins (Triglidae), and assemblages like icefishes (Notothenioidei), sculpins, and snailfishes (Cottoidei), eelpouts (Zoarcoidei) and scorpionfishes (Scorpaenoidei) (Wiley et al., 2000, Chen, 2001, Chen et al., 2003, Miya et al., 2003, Miya et al., 2005, Dettai and Lecointre, 2004, Dettai and Lecointre, 2005, Dettai and Lecointre, 2008, Smith and Wheeler, 2004, Smith and Wheeler, 2006, Smith and Craig, 2007, Li et al., 2009, Matschiner et al., 2011, Near et al., 2012). Yet these groups have been recovered time and time again by multiple studies performed by different teams and with different species and samples. It is now time to start taking seriously the clades that have been repeatedly corroborated, and to explore them in more detail. This has been started already on some groups, and we are here going to explore relationships within Serraniformes (Li et al., 2009) using a denser sampling and additional markers.
For the name and content of the species, families, suborders and orders, we will follow Nelson (2006).
Very reduced versions of the group started to appear in molecular phylogenies in the early 2000 (Wiley et al., 2000, Chen, 2001, Chen et al., 2003, Miya et al., 2003, Miya et al., 2005, Orrell et al., 2006). More complete versions with a better taxonomic coverage were published in Dettai and Lecointre, 2004, Dettai and Lecointre, 2005, Smith and Wheeler, 2004, Smith and Wheeler, 2006, Li et al., 2009. In this diverse and particularly interesting assemblage of families, some are important for world fisheries (groupers) or toxin evolution (mail-cheeked fishes); others have been used as developmental and genomic models (sticklebacks) or possess unique evolutionary biochemical and physiological traits (nototheniids, channichthyids).
From 8 to 28 families have been included in analyses of the Serraniformes depending on the sampling of the molecular study considered (Miya et al., 2003, Dettai and Lecointre, 2005, Smith and Wheeler, 2006, Li et al., 2009). While there is little contradiction among the studies, this lack of overlap makes assessment of corroboration across studies more difficult, and the composition of the clade remains to be checked with a better sampling of acanthomorphs. Serraniformes are an assemblage of some members, but not all, of several previously used Acanthomorph orders (Nelson, 2006). From Gasterosteiformes, they only include sticklebacks (Gasterosteidae) and aulorhynchids (Smith and Wheeler, 2004, Smith and Wheeler, 2006, Li et al., 2009), while the other members of the Gasterosteiformes are reliably grouped with other clades. Many Perciform families are members of the Serraniformes: wolffishes (Anarhichadidae), perches (Percidae), gunnels (Pholidae), groupers (Serranidae), weeverfishes (Trachinidae), eelpouts (Zoarcidae), icefishes, Antarctic dragon-fish or plunderfish (Notothenioidei) (Smith and Wheeler, 2004, Smith and Wheeler, 2006, Smith and Craig, 2007, Li et al., 2009, Matschiner et al., 2011, Near et al., 2012, Wainwright et al., 2012), while again, all the other tested families from this polyphyletic order are reliably grouped with other clades. All Scorpaeniformes tested to this day appear to belong in Serraniformes, whether they were part of the Cottoidei, the Scorpaenoidei or the Hexagrammoidei: poachers (Agonidae), sculpins (Cottidae), pigfishes (Congiopodidae), lumpfishes (Cyclopteridae), snailfishes (Liparidae), fatheads (Psychrolutidae), scorpionfishes (Scorpaenidae), searobins (Triglidae) (Smith and Wheeler, 2004, Smith and Wheeler, 2006, Smith and Craig, 2007, Li et al., 2009, Near et al., 2012), but the combinations are new and the suborders are not all regrouped. Gasterosteiformes, Perciformes, and Scorpaeniformes are therefore para- or polyphyletic, as had already been suggested by morphological studies, albeit not always with the same groupings (Johnson and Patterson, 1993, Imamura and Yabe, 2002). For most of these groups, non-monophyly is not surprising. Perciformes never received a clear definition (Nelson, 2006). Some scorpaeniforms appear to be included in Perciformes (Johnson and Patterson, 1993, Mooi and Gill, 1995; but see review of Shinohara & Imamura, 2007). Inversely, several families belonging to the Perciformes might be included within Scorpaeniformes, like Champsodontidae (Mooi & Johnson, 1997). To explore Serraniformes, a large and representative sampling of both Perciformes and Scorpaeniformes is therefore necessary. At a smaller scale, some families present monophyly issues: Serranidae (Schoelinck et al., in preparation, Smith and Craig, 2007), Nototheniidae (Dettai et al., 2012), and Scorpaenidae (Smith and Wheeler, 2004, Li et al., 2009) are not monophyletic. However, the evaluation at this scale needs a fine-grained taxonomic sampling. By including as many families as possible from these groups, as well as multiple outgroups, we provide a clearer picture of which groups are really included in the Serraniformes, and what the relationships within this group are.
Marker choice has a high importance for the reliability and relevance of phylogenetic studies. Several studies showed that IRBP (interphotoreceptor retinoid-binding protein) (Dettai and Lecointre, 2008, Chen and Mayden, 2009), MLL4 (Mixed-lineage leukemia-like protein 4) (Dettai & Lecointre, 2005), Rhodopsin retrogene (Chen et al., 2003) and RNF213 (ring finger protein 213) (Li et al., 2009) are relevant for the large scale phylogeny of acanthomorphs. However, these markers have not resolved many of the relationships sufficiently or convincingly. While previous studies have provided valuable results on a limited number of markers, new and suitable nuclear markers are still needed to increase accuracy and resolution.
We selected Pkd1 (polycystic kidney disease) used previously only at a small scale (Lautredou et al., 2010, Lautredou et al., in press). The gene Pkd1 encodes a glycoprotein, but its function is unclear except that it is involved in adhesive cell–cell/matrix interactions (Gluecksmann-Kuis et al., 1995). We also selected MC1R (melanocortin type 1 receptor), a protein involved in changes of body pigmentation in many groups (Mundy, 2005, Rosenblum et al., 2004, Healy et al., 2001) including teleosts (Logan et al., 2003b, Gross et al., 2009). It has been used for phylogeny in primates (Mundy & Kelly, 2003) and cichlids (Henning et al., 2010).
Genome sequencing has created a wealth of new information for scientists to analyze, and genome/genome comparison allows to easily define and test new markers (Li et al., 2007, Li et al., 2009). We included one new nuclear marker, MLL2 (Mixed-lineage leukemia-like protein 2), a histone methyltransferases (HMTs) (Yu et al., 1998, Hess, 2004, Ansari et al., 2008). While Pkd1, MC1R, and MLL2 are extensively studied for their function, little is known about their evolution and diversity in most groups. Acquiring sequences for a large diversity of species over an important group like acanthomorphs has an interest not only for the phylogenetic resolution it provides, but is also essential to make hypotheses about the evolution of protein structure and to improve the accuracy of functional classification (Rost, 1999, Sjolander, 2004, Jaroszewski et al., 2009, Godzik, 2011).
The first objective of this study is to assess the variability of the seven markers used in this study by comparing their divergence between chosen pairs of taxa with other nuclear markers used in teleosts (Chen et al., 2003, Smith and Wheeler, 2004, Smith and Wheeler, 2006, Li et al., 2007, Smith and Craig, 2007). The second objective is to use these markers (with a focus on Pkd1, MC1R and MLL2, never used for Serraniformes) to test the monophyly of clades within Serraniformes, especially Scorpaenidae and Serranidae, and provide phylogenetic hypotheses within the clade. New insights on the relationships within Serraniformes could change our interpretation of the evolution of Antarctic teleosts (Chen et al., 2003), of venom evolution (Nelson, 2006, Smith and Wheeler, 2006), and could bring a new light on the distribution of morphological characters, especially in Scorpaenidae.
Section snippets
Gene sampling
Seven protein-coding markers were used in this study. Four have already been used for large scale phylogenies on Acanthomorpha: IRBP, MLL4, Rhodopsin retrogene and RNF213. Pkd1, MLL2 and MC1R have never been used before in Serraniformes. They were developed with a protocol described in Li et al. (2009) and Lautredou et al. (2012).
New primers have been developed here for MLL4, RNF213, MC1R, MLL2 and Pkd1. Some of them were aimed at Serranidae (MLL2F100-MLL2R945, Pkd1F51b-Pkd1R737) or
Results and discussion
Except for Pkd1, the new primers outperformed the older ones (see * in Table 1). In total, 130 specimens could be sequenced for IRBP (66%), 142 for MLL4 (72%), 160 for Rhodopsin (81%), and 131 for RNF213 (67%). Concerning the new markers, 133 specimens were sequenced for Pkd1 (67%), 114 for MC1R (58%), and 134 for MLL2 (68%). Among our specimens, MC1R had the lowest percentage of successful sequencing; however, no sucessful new primers were designed for this marker. Even without new primers,
Conclusion
The addition of taxa is important to resolve taxonomic issues. As there are numerous markers in this study as well as a good sampling, the present study can assess the relationships among the families belonging to the Serraniformes, as well as the monophyly or non-monophyly of the different families of this group. We confirm some previous results but also question some others. The clades D and E are very well supported and recovered in several studies. The sister-relationship of Percophidae and
Acknowledgments
This work was supported by a TOTAL Fundation grant. We also thank Christina Cheng, Samuel Iglesias, Jean-Lou Justine, Charlotte Schoelinck, the Museum Victoria, the University of Kansas, the Moorea Biocode Project, the CEAMARC, SANTO and EVOHE cruises for the tissue samples. We thank the ‘Service de systematique moleculaire’ (IFR CNRS 101) of the ‘Muséum national d’histoire naturelle’, Paris, France, for support; the Barcode and the ‘Bibliotheque du Vivant’ projects for the sequencing. We thank
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