Phylogeny and Taxonomy of Flatheads, Scorpionfishes, Sea Robins, and Stonefishes (Percomorpha: Scorpaeniformes) and the Evolution of the Lachrymal Saber
We report on the discovery of a remarkable defensive specialization in stonefishes that was identified during a phylogenetic study of scorpionfishes and their relatives. This newly described innovation, the lachrymal saber, involves modifications to the circumorbitals, maxilla, adductor mandibulae, and associated tendons. At its core, the lachrymal saber is an elongation of an anterior spine (or spines) on the ventral surface of the lachrymal that stonefishes are capable of rotating from the standard ventral position to a locked lateral position. The locking mechanism minimally includes a bony spur on the inner surface of the lachrymal and a ridged bony protuberance on the anterolateral end of the maxilla. A modified and highly subdivided adductor mandibulae appears to control the movement of the lachrymal saber by rotating the maxilla while it is engaged with the spur on the medial side of the lachrymal. This maxillary rotation results in a subsequent rotation of the lachrymal that we hypothesize reduces predation on stonefishes. This specialization was included in our phylogenetic analysis of scorpaenoid fishes. This study expands upon the previous higher-level taxonomic sampling reported in earlier evolutionary studies of scorpaenoid fishes and, unlike previous analyses, explicitly combines molecular and morphological data with an expanded taxonomic sampling to mitigate the conflict between these competing datasets. The resulting phylogeny based on a combination of 113 morphological and 5,280 molecular characters for 63 species is used to produce a revised taxonomy of flatheads, scorpionfishes, sea robins, and stonefishes. Our results do not support the monophyly of the traditional Scorpaeniformes, Scorpaenoidei, Scorpaenoidea, Platycephaloidea, Bembridae, Scorpaenidae, Sebastidae, Serranidae, Tetrarogidae, or Triglidae. Our monophyletic taxonomy recognizes nine monophyletic families: Bembridae, Congiopodidae, Hoplichthyidae, Neosebastidae, Platycephalidae, Plectrogeniidae, Scorpaenidae, Synanceiidae, and Triglidae. The taxonomic composition of the Congiopodidae, Hoplichthyidae, Neosebastidae, and Platycephalidae are unchanged. The Bembridae is expanded to include the recently described Parabembridae, while Bembradium is moved to the Plectrogeniidae. The Scorpaenidae is expanded to include the traditional Sebastidae and Setarchidae. The Triglidae is expanded to include the Peristediidae. Finally, a revised Synanceiidae, diagnosed by the lachrymal saber, is expanded to include the Apistidae, Aploactinidae, Eschmeyeridae, Gnathanacanthidae, Pataecidae, Perryenidae, and Tetrarogidae. Based on these results, we recommend treating all of these traditional scorpaenoid clades as families in an expanded Scorpaeniformes that includes a restricted Scorpaenoidei that includes all traditional scorpaenoid families except the Congiopodidae. The resulting phylogeny is then used to explore aspects of scorpaenoid evolution.
Morphological hypotheses of inter- and intrafamilial relationships of the scorpaenoid lineage and allies: (A) traditional scorpaeniforms (Matsubara, 1943); (B) scorpionfishes and allies (Matsubara, 1943); (C) Scorpaenoidea (Imamura, 2004); (D) Scorpaenoidei (Ishida, 1994).
Molecular hypotheses of inter- and intrafamilial relationships of the scorpaenoid lineage and allies: (A) Scorpaenoidei and allies (Smith and Craig, 2007); (B) traditional Scorpaeniformes and allies (Lautredou et al., 2013; * indicates probable problematic placement—see Smith and Busby [2014] for discussion).
Optimal cladogram resulting from the partitioned likelihood analysis of the dataset composed of 113 phenotypic and 5,280 nucleotide characters. Clades with 50% bootstrap support are retained and identified with their support. Nodes with bootstrap support of 95% were marked with an “*”. Family-level classification is designated on the right. Dashed branches indicate terminals that were represented only by morphological data that were excluded from the bootstrap analyses. Family-level-phylogeny of scorpaenoids and their sister group in gray box in upper-right corner.
Lateral view of a cleared-and-stained specimen of the synanceiid Paracentropogon, CAS_SU 68769. Images highlight the (A) resting position of the lachrymal saber (arrow) along the side of the waspfish's cheek and the (B) locked-out position where the lachrymal saber extends laterally from the specimen. The rotation of both the first and second circumorbital are visible in the lower image.
Lateral (A), rostral (B), and dorsal (C) views of the lachrymal saber in the Soldierfish (Gymnapistes marmoratus, AMNH 31009). Arrow highlights both the resting and locked lachrymal saber in the various angles.
Skeletal images of the key lachrymal saber components. (A) Lateral image of the lachrymal, second circumorbital (CO2), and third circumorbital (CO3) in Minous quincarinatus, KUI 41397. Circular inset of upper image shows medial view with medial protuberance (PP). (B) Lateral image of the maxilla in Apistus carinatus, KUI 41400. Circular inset of lower image shows closeup of the maxillary protuberance (MP). These two protuberances interact to lock the lachrymal saber.
Composite dorsal images of various specimens of Paracentropogon highlighting the morphology of the components of the lachrymal saber with the locked position on the left side and the resting position on the right side. Note that the anteriormost component of the palatine has been made largely transparent in the images to allow for a better examination of the maxilla. The upper image (A) represents the anatomy with all elements marked, and the lower image (B) represents the image with the circumorbitals shadowed to visualize underlying muscles. Muscle attachments on removed bones are denoted with pale circles at the interface. Abbreviations: A1 or A2 represent the major subdivisions of the adductor mandibulae; CO3–circumorbital 3; CO4–circumorbital 4; LAP–levator arcus palatini; MP–maxillary protuberance. Illustration by Clara Richardson.
Lateral view of the non-circumorbital components of the lachrymal saber in composite images of the various specimens of Paracentropogon above (A) and the various specimens of Apistus below (B). The comparisons are shown to illustrate variation in this system between species (e.g., subdivisions and attachment points of the adductor mandibulae). Muscle attachments on removed bones are denoted with pale circles at the interface. Abbreviations: A1 or A2 represent the major subdivisions of the adductor mandibulae; LAP–levator arcus palatini; MP–maxillary protuberance. Illustration by Clara Richardson.
Lateral (A and B) and rostral (C) images of Centropogon australis, KUI 41409. (A) Image represents a visible light image of Centropogon with the lachrymal saber in the resting position. (B) Image represents the identical placement of the image in panel A under fluorescent light with GFP filter under the Nikon SMZ-18 microscope. This image shows the bright green biofluorescence visible on the lachrymal saber. (C) Image shows a rostral view of the same individual under NightSea BlueStar flashlight illumination and the light-shading plate from the Nikon SMZ-18, which is not as restricted as the microscope filter. In this image, the green (lachrymal saber) and orange (dorsal surface of head) fluorescent emissions are visible in the waspfish.
Contributor Notes
Associate Editor: T. Grande.