Data collection, alignment, model choice, and morphological characters.—DNA sequence data used in this study (Table 1) includes newly collected (GenBank accession numbers KM983049–KM983094) and previously published sequences (Davis, 2010; Near et al., 2012; Davis et al., 2014). Taxonomic sampling for DNA-only analyses included ten species (of 18) representing all scopelarchid genera, with the total evidence approach incorporating an additional three species. Combinations of mitochondrial and nuclear genes have been demonstrated to provide significant phylogenetic resolution in fishes (e.g., Chakrabarty et al., 2011a, 2011b; Li et al., 2011; McMahan et al., 2013b; Sparks et al., 2014). Mitochondrial and nuclear genes were aligned using the program MAFFT v6.0 with default parameters (Katoh et al., 2002). The phylogenetic analyses presented herein had a total of 7,137 base pairs, including one mitochondrial gene (cytochrome oxidase I, 812 bp) and seven protein-coding genes (ectodermal-neural cortex 1-like gene, 845 bp; glycosyltransferase gene, 839 bp; myosin heavy chain 6 alpha gene, 759 bp; pleiomorphic adenoma protein-like 2-like gene, 819 bp; ptr hypothetical protein, 767 bp; recombination activating gene 1, 1449 bp; zic family member protein, 847 bp). For each maximum likelihood analysis, the dataset was partitioned by individual gene codons, for a total of 24 partitions. Models of molecular evolution were chosen by the program jMODELTEST v.2.1 (Posada, 2008), with the best fitting model under the Akaike information criteria (AIC) for each individual gene and codon partition assigned, including: cytochrome oxidase I (TIM1+Γ, HKY, GTR+I+Γ), ectodermal-neural cortex 1-like gene (Trn, TVM, TPM1uf), glycosyltransferase (HKY+Γ, TPM1uf+I+Γ, GTR+I), myosin heavy chain 6 alpha (TIM1+I, F81+G, TVM), pleiomorphic adenoma protein-like 2-like gene (HKY, TrN, TPM1uf+Γ), ptr hypothetical protein (TIM1+Γ, GTR+I, TPM1uf+Γ), recombination activating gene 1 (TPM1uf+I, HKY+G, TVM+G), and zic family member protein (F81, HKY, HKY+Γ).

Table 1.

GenBank accession numbers for DNA data. Gene abbreviations: COI  =  cytochrome oxidase I; ENC1  =  ectodermal-neural cortex 1-like gene; glyt  =  glycosyltransferase gene; myh6  =  myosin heavy chain 6 alpha gene; plagl2  =  pleiomorphic adenoma protein-like 2-like gene; Ptr  =  ptr hypothetical protein; rag1  =  recombination activating gene 1; zic1  =  zic family member protein 1.

Total evidence analyses included an additional partition (MK model, Lewis, 2001) incorporating data from 14 morphological and early-life-history characters used to infer the evolutionary relationships among scopelarchid taxa in Johnson (1974) and two additional characters presented herein for a total of 16 morphological characters. Abbreviated character descriptions from Johnson (1974) are found in Appendix 1. For further details regarding these character states, please refer to Johnson (1974). Character state codings for species are listed in Table 2.

Table 2.

Morphological data matrix of 16 anatomical and early life history characters from Johnson (1974) and this study. Refer to text for further details regarding characters.

Topology and character state reconstruction.—Maximum likelihood analyses were performed in GARLI v2.01 (Zwickl, 2006). Five analyses were conducted for both the DNA-only and total evidence analyses, and the trees having the best likelihood scores are presented here to evaluate evolutionary relationships. A nonparametric bootstrap analysis (Felsenstein, 1985) was performed for each dataset with 100 random pseudoreplicates using the recommended default settings in the GARLI manual. Ancestral character state reconstruction was performed in Mesquite v.2.75 (Maddison and Maddison, 2010) with maximum parsimony methodology, and distributional data for taxa are based on results presented in Johnson (1974, 1982) and specimen occurrence data in the Global Biodiversity Information Facility (2014, www.gbif.org).

Type species.—Lagiacrusichthys macropinnis

Diagnosis.—The genus Lagiacrusichthys can be distinguished from all other members of Scorpelarchidae based on the unique combination of the following characters modified from Bussing and Bussing (1966) and Johnson (1974): long anal fin with 35–39 anal-fin rays (17–30 in other species of Scopelarchidae); dorsal fin small and approximately same size or smaller than adipose fin, with a low dorsal-fin ray count of 5–6 (6–10 in other species of Scopelarchidae).

Habitat and distribution.—Found predominantly in marine waters in the southern hemisphere with a circumpolar distribution in the Antarctic Circumpolar Current (Bussing and Bussing, 1966; Johnson, 1974; Post, 1990). Collected predominantly from deep-sea open ocean environments (meso-bathypelagic) at depths ranging from 610–2750 meters (Bussing and Bussing, 1966; Johnson, 1974).

Etymology.—Named for a wyvern, a dragon-like creature from mythology, specifically the sea-wyvern Lagiacrus, known for his fierceness and for inhabiting the deep. Treated as masculine.

Phylogenetic placement of Lagiacrusichthys and relationships within Scopelarchidae.—The inferred evolutionary relationships among scopelarchid genera were the same for both DNA-only (Fig. 2) and total evidence analyses (Fig. 3). Bootstrap values and unambiguous synapomorphies supporting clades are indicated in Figure 3, following the recommendation of Wiley et al. (2011). The genus Benthalbella was identified as the stem pearleye lineage. Four unambiguous synapomorphies support the monophyly of Benthalbella (Fig. 3), including the absence of antorbital bones (5∶1), a reduced supramaxilla (6∶1), an abrupt timing of larval metamorphosis (9∶2), and the appearance of pelvic-fin buds anterior to the dorsal fin in larvae (10∶1). Benthalbella is the sister group to a clade that includes Rosenblattichthys as the sister group to a clade that includes Lagiacrusichthys, Scopelarchoides, and Scopelarchus (Figs. 2, 3). The monophyly of Rosenblattichthys is supported by two unambiguous synapomorphies (Fig. 3) concerning the early life history of fishes in this lineage, including pectoral fin development precocious in larvae (11∶1) and noticeably enlarged heads in larvae (12∶1). Lagiacrusichthys is the sister group to a Scopelarchus and Scopelarchoides clade. Lagiacrusichthys has two unreversed and unambiguous autapomorphies that differentiate it from all other scopelarchid taxa (Fig. 3), including a significantly long anal fin (15∶1) and a significantly reduced dorsal fin (16∶1).

Fig. 2.

Evolutionary relationships of the pearleyes (Scopelarchidae) based on eight gene fragments and maximum likelihood topology estimation. Numbers by nodes indicate bootstrap values. Representative line drawings of genera are based on specimens examined and modifications from prior illustrations (Johnson, 1974; Bussing and Bussing, 1966).

Fig. 3.

Evolutionary relationships of the pearleyes (Scopelarchidae) based on total evidence (eight gene fragments and 16 anatomical and early-life-history characters) from maximum likelihood topology estimation. Asterisks indicate taxa that do not have DNA data. Bold numbers by nodes indicate bootstrap values. Numbers near circles on branches indicate unambiguous synapomorphies, with the first number corresponding to one of the 16 anatomical and early-life-history characters (see text for details), with the second number indicating character state. White circles represent unreversed characters, while black circles represent homoplastic characters. Colors on branches and distribution map correspond to the regions of the oceans where each species has been predominantly collected (note that many species have more restricted ranges within these zones). Circles at nodes indicate results from parsimony ancestral character reconstruction of regions (green: boreal and subarctic waters of North Pacific, orange: central-tropical waters, blue: Antarctic waters).

The genera Scopelarchoides and Scopelarchus were inferred to be sister groups (Figs. 2, 3), with one unambiguous synapomorphy supporting this clade: the absence of parietal bones (1∶1). There are no unambiguous morphological synapomorphies that support the monophyly of Scopelarchoides, although this clade is well supported by molecular data (Figs. 2, 3). Three unambiguous synapomorphies support the monophyly of Scopelarchus (Fig. 3). These include the absence of antorbital bones (5∶1), the absence of a posterior arm on the hyomandibular bone (13∶1), and unarranged dermal pigment spots on the body (14∶1).

Relationships of the pearleyes (Scopelarchidae).—This work represents the most taxonomically comprehensive molecular phylogeny of the family Scopelarchidae to date, including representatives from all four previously recognized genera and the newly recognized Lagiacrusichthys. Previous molecular studies on aulopiform fishes (Davis, 2010; Davis and Fielitz, 2010) have included only a single representative for three pearleye genera (Benthalbella, Lagiacrusichthys, and Scopelarchus), and recent morphological studies into the evolutionary relationships of aulopiform fishes (Baldwin and Johnson, 1996) inferred a polytomy among the four scopelarchid genera recognized at that time (Benthalbella, Rosenblattichthys, Scopelarchus, and Scopelarchoides). Results from the DNA-only and total evidence analyses (Figs. 2, 3) infer the same pattern of evolutionary relationships among the five scopelarchid genera, with Benthalbella identified as the stem pearleye lineage. Of the remaining four scopelarchid genera, Rosenblattichthys is inferred to be the sister group to a clade that includes Lagiacrusichthys sister to a clade including the genera Scopelarchoides and Scopelarchus (Figs. 2, 3).

The taxon Lagiacrusichthys macropinnis was initially placed within Benthalbella (e.g., Bussing and Bussing, 1966; Johnson, 1974, 1982) based primarily on its elongated body and the presence of pelvic fins that are anterior to the base of the dorsal fin. Earlier studies on the relationships and taxonomy of scopelarchid taxa (Marshall, 1955; Rofen, 1966) identified a significant distinction between two body types within the pearleyes (of which only three genera were diagnosed at that time): an elongated body form with pelvic fins anterior to the base of the dorsal fin (Benthalbella) and a comparatively shorter body form with pelvic fins posterior to the base of the dorsal fin (Scopelarchus, Scopelarchoides). Newly considered molecular evidence presented here indicates that the Antarctic Pearleye (Lagiacrusichthys macropinnis) represents a distinct lineage from the other four described species of Benthalbella (Figs. 2, 3). This finding is also supported by a number of anatomical and early-life-history characters (Fig. 3). The Antarctic Pearleye (Lagiacrusichthys macropinnis) has two unreversed and unambiguous autapomorphies that differentiate it from all other scopelarchid taxa (Fig. 3), including a long anal fin (15∶1) and a reduced dorsal fin (16∶1). While Lagiacrusichthys macropinnis and species of Benthalbella share pelvic fins that are anterior in position to the origin of the dorsal fin, the development of these pelvic fin positions differ significantly between the two genera, with Benthalbella having pelvic-fin buds that appear entirely anterior to the dorsal-fin origin in larvae (10∶1). In Lagiacrusichthys, the pelvic-fin buds appear posteriorly to the dorsal-fin origin in larvae (10∶0), as they do in all other scopelarchid taxa (with the exception of Benthalbella).

The circumglobal distribution of Scopelarchidae in meso-bathypelagic environments.—Johnson (1974) hypothesized that the common ancestor of the family Scopelarchidae most likely evolved in central-tropical marine waters, with various invasions into boreal and subarctic waters of the North Pacific (Benthalbella) and Antarctic south of Subtropical Convergence (Benthalbella and Lagiacrusichthys). Based on the evolutionary relationships presented herein (Fig. 3), it is inferred that the common ancestor of the pearleyes most likely evolved in central-tropical waters, and the majority of pearleye diversity is found in these environments. Two independent invasions into Antarctic waters are identified within the scopelarchids: once in Benthalbella (B. elongata, Southern Pearleye), and once in Lagiacrusichthys (L. macropinnis, Antarctic Pearleye). Two species within Benthalbella (B. linguidens and B. dentata) are restricted to boreal and subarctic waters of the North Pacific (Fig. 3), although further molecular and morphological data collection is needed to clearly resolve the relationships among the four species in Benthalbella, which would aid in inferring the number of independent invasions into the North Pacific or central-tropical waters. At present, the results from the parsimony ancestral character reconstruction of regions identify that a North Pacific or central-tropical ancestor is an equally parsimonious possibility for the common ancestor of Benthalbella.