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Phylogeny and Taxonomy of Sculpins, Sandfishes, and Snailfishes

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Phylogeny and Taxonomy of Sculpins, Sandfishes, and Snailfishes Molecular Phylogenetics and Evolution 79 (2014) 332–352 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny and taxonomy of sculpins, sandfishes, and snailfishes (Perciformes: Cottoidei) with comments on the phylogenetic significance of their early-life-history specializations ⇑ W. Leo Smith a, , Morgan S. Busby b a Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USA b Alaska Fisheries Science Center, National Marine Fisheries Service, 7600 Sand Point Way NE, Seattle, WA 98115, USA article info abstract Article history: Despite recent progress on the higher-level relationships of the Cottoidei and its familial components, Received 24 April 2014 phylogenetic conflict and uncertainty remain within the Cottoidea. We analyzed a dataset composed Revised 27 June 2014 of 4518 molecular (mitochondrial 12S, tRNA-Val, 16S, and cytochrome b and nuclear TMO-4c4, Histone Accepted 30 June 2014 H3, and 28S) and 72 morphological characters for 69 terminals to address cottoid intrarelationships. The Available online 8 July 2014 resulting well-resolved phylogeny was used to produce a revised taxonomy that is consistent with the available molecular and morphological data and recognizes six families: Agonidae, Cottidae, Jordaniidae, Keywords: Psychrolutidae, Rhamphocottidae, and Scorpaenichthyidae. The traditional Agonidae was expanded to Scorpaeniformes include traditional hemitripterids and Hemilepidotus. The traditional Cottidae was restricted to Leptocot- Perciformes Mail-cheeked fishes tus, Trachidermus, and the riverine, lacustrine, and Lake Baikal freshwater cottoids. Jordaniidae (Jordania Reproduction and Paricelinus) was separated from the traditional cottids; Psychrolutidae was expanded from the Larvae traditional grouping to include nearly all traditional marine cottids and the single species of bathy- lutichthyid. Rhamphocottidae was expanded to include the traditional ereuniids, and Scorpaenichthyidae separated Scorpaenichthys from the traditional cottids. The importance of early-life-history characters to the resulting phylogeny and taxonomy were highlighted. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction Agonidae (Smith and Wheeler, 2004), Cottocomephoridae (Hunt et al., 1997; Kontula et al., 2003; Kinziger et al., 2005), Cottidae 1.1. Cottoid background (Hunt et al., 1997; Jackson, 2003; Kontula et al., 2003; Smith and Wheeler, 2004; Crow et al., 2004; Kinziger et al., 2005; Smith, The cottoid fishes (sculpins, sandfishes, and snailfishes) are one 2005; Knope, 2013), and Hemitripteridae (Smith and Wheeler, of the largest and most morphologically diverse teleostean subor- 2004; Smith, 2005; Knope, 2013), and they have often recovered ders with more than 825 species classified in 7–20 families (Jordan, the Bathylutichthyidae (Smith, 2005), Comephoridae (Hunt et al., 1923; Washington et al., 1984; Yabe, 1985; Smith and Wheeler, 1997; Kontula et al., 2003; Smith and Wheeler, 2004; Kinziger 2004; Eschmeyer, 2014). Despite progress on cottoid inter- and et al., 2005; Smith, 2005), Cyclopteridae (Jackson, 2003; Smith intrarelationships during the last 30 years following the ground- and Wheeler, 2004), Liparidae (Jackson, 2003; Smith and breaking work of Yabe (1985), problems with their taxonomy Wheeler, 2004), and Psychrolutidae (Jackson, 2003; Smith and remain (Hunt et al., 1997; Jackson, 2003; Kontula et al., 2003; Wheeler, 2004; Smith, 2005; Knope, 2013) nested within the Smith and Wheeler, 2004; Crow et al., 2004; Imamura et al., Cottidae. In short, the limits of the various cottoid families need 2005; Kinziger et al., 2005; Smith, 2005; Knope, 2013). These stud- revision. ies have variously refuted the monophyly of the Abyssocottidae Biologically, the cottoid radiation is perhaps best known for its (Hunt et al., 1997; Kontula et al., 2003; Kinziger et al., 2005), diverse reproductive modes and early-life-history specializations (Breder and Rosen, 1966; Washington et al., 1984; Abe and Munehara, 2009; Muñoz, 2010). Typically, cottoids and their close ⇑ Corresponding author. Address: Biodiversity Institute, 1345 Jayhawk Blvd., allies in the Zaniolepididae and Hexagrammidae spawn demersal University of Kansas, Lawrence, KS 66045, USA. eggs (Matarese et al., 1989). Further, many sculpins provide paren- E-mail addresses: [email protected] (W.L. Smith), [email protected] tal care or deposit their eggs in concealed spaces or cavities (e.g., (M.S. Busby). http://dx.doi.org/10.1016/j.ympev.2014.06.028 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. W.L. Smith, M.S. Busby / Molecular Phylogenetics and Evolution 79 (2014) 332–352 333 within the tissues of various invertebrates; Marliave, 1978; 1.3. Cottoid intrarelationships Munehara et al., 1991; Busby et al., 2012). Along with these behav- ioral modifications, cottoids have developed reproductive modifi- Cottoidei is the largest suborder of traditional mail-cheeked cations that allow for specializations ranging from live birth in fishes. This group has approximately 833 species (Eschmeyer, some Lake Baikal sculpins (Comephorus), to copulation, to internal 2014) spread among 139 genera that are currently classified in gametic association with external fertilization in some sculpins, nine families: Agonidae (46 spp.), Cottidae (289 spp.), Cyclopteri- sea ravens, and poachers (e.g., Munehara et al., 1991, 1997; dae (27 spp.), Ereuniidae (3 spp.), Hemitripteridae (8 spp.), Petersen et al., 2004, 2005; Muñoz, 2010). Internal gametic associ- Liparidae (416 spp.), Psychrolutidae (41 spp.), Rhamphocottidae ation involves the joining of eggs and spermatozoa in the ovary (1 sp.), and Trichodontidae (2 spp.). This classification follows with fertilization occurring after the eggs are deposited in seawater Yabe (1985) with the following recommendations by Smith and (Munehara et al., 1991, 1997; Busby et al., 2012). Once fertilized, Wheeler (2004) and/or Smith (2005): inclusion of trichodontids cottoid young often have heavy spination, the development of (previously in the Trachinoidei) in Cottoidei, inclusion of the armor, and precocious development in which flexion occurs within Bathylutichthyidae in Psychrolutidae, and the inclusion of abysso- the egg (Matarese et al., 1989; Busby and Ambrose, 1993; Busby, cottids, comephorids, and cottocomephorids in Cottidae. Regan 1998). These morphological and behavioral modifications are all (1913) first united this cottoid assemblage (less Trichodontidae) strategies that have the potential to increase survivorship of the as the Cottiformes, an order of his Scleroparei. He used the reduc- eggs, larvae, and juveniles. tion in size of the endopterygoid (his mesopterygoid) and interca- lar (his opisthotic) and the loss of the basisphenoid to differentiate 1.2. Cottoid interrelationships this taxon from other mail-cheeked fishes. Later, Jordan (1923), Berg (1940), Matsubara (1943), Quast (1965) and Greenwood Historically, cottoid fishes and their close relatives in the Hexa- et al. (1966) retained this assemblage in their classifications look- grammoidei, Zaniolepidoidei, and Anoplopomatoidei have been ing at various aspects of teleostean phylogeny. classified with the scorpionfishes and allies in the Scorpaeniformes Taranetz (1941) and Bolin (1947) provided the first detailed (Greenwood et al., 1966; Washington et al., 1984; Imamura and morphological surveys of the cottoids. Taranetz (1941) examined Shinohara, 1998; Nelson, 2006). However, recent work (Yabe and species across the Cottoidei and provided a wealth of anatomical Uyeno, 1996; Imamura and Yabe, 2002; Chen et al., 2003; Miya data to justify his classification. Unfortunately, his study suffered et al., 2003; Smith and Wheeler, 2004, 2006; Smith and Craig, from the use of inexplicit methods and a proliferation of family- 2007; Lautredou et al., 2013) has demonstrated that the eelpouts level names that has often complicated cottid taxonomy. Bolin (Zoarcoidei) or sticklebacks (Gasterosteioidei), not the scorpaenoid (1947; Fig. 1B) provided a ‘‘phylogenetic tree’’ of the cottids of lineage, are the closest relatives to the Cottoid Lineage (reviewed in California that utilized his own evolutionary methods. Bolin’s Smith and Wheeler (2004) and Lautredou et al. (2013)). Further, hypothesis shares many similarities with recent phylogenetic Smith and Wheeler (2004), Imamura et al. (2005) and Smith hypotheses (Yabe, 1985; Smith and Wheeler, 2004), but its global (2005) have provided morphological and molecular evidence or taxonomic conclusions were hampered by its restriction to species both to support the placement of the Trichodontidae in an in California and its lack of key cottoid groups (e.g., Agonidae, expanded Cottoidei. Recent studies now consistently recover this Psychrolutidae). expanded Cottoid Lineage among the scorpionfishes and seabasses Washington et al. (1984; Fig. 1C) provided the first phylogenetic (Scorpaenoidei), perches and icefishes (Percoidei), sticklebacks analysis of the Cottoidei. Their study, which briefly summarizes the (Gasterosteioidei) and eelpouts (Zoarcoidei) in a clade that is most hypothesized apomorphic states of 47 characters, was based on an similar to an expanded Scorpaeniformes (Smith and Craig, 2007; unpublished manuscript by Washington and Richardson. This phy- Near et al., 2012, 2013; Lautredou et al., 2013; Wainwright et al., logeny separated their Cyclopteridae (Cyclopteridae + Liparidae) 2012; Betancur-R et al., 2014). from
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