An enigmatic pelagic fish with internalized red muscle: A future regional endotherm or forever an ectotherm?

Ectothermy and endothermy in extant fishes are defined by distinct integrated suites of characters. Although only ⁓0.1% of fishes are known to have endothermic capacity, recent discoveries suggest that there may still be uncommon pelagic fish species with yet to be discovered endothermic traits. Among the most rarely encountered marine fishes, the louvar Luvarus imperialis is a remarkable example of adaptive evolution as the only extant pelagic species in the order Acanthuriformes (including surgeonfishes, tangs, unicornfishes and Moorish idol). Magnetic resonance imaging and gross necropsy did not yield evidence of cranial or visceral endothermy but revealed a central-posterior distribution of myotomal red muscle that is a mixture of the character states typifying ectotherms (lateral-posterior) and red muscle endotherms (central-anterior). Dissection of a specimen confirmed, and an osteological proxy supported, that L. imperialis has not evolved the vascular rete that is vital to retaining heat in the red muscle. The combination of presumably relying on caudal propulsion while exhibiting internal red muscle without associated retia is unique to L. imperialis among all extant fishes, raising the macroevolutionary question of whether this species - in geologic timescales - will remain an ectotherm or evolve red muscle endothermy.

Quantitative Classification of Cerebellar Foliation in Cartilaginous Fishes (Class: Chondrichthyes) Using Three-Dimensional Shape Analysis and Its Implications for Evolutionary Biology.

A true cerebellum appeared at the onset of the chondrichthyan (sharks, batoids, and chimaerids) radiation and is known to be essential for executing fast, accurate, and efficient movement. In addition to a high degree of variation in size, the corpus cerebellum in this group has a high degree of variation in convolution (or foliation) and symmetry, which ranges from a smooth cerebellar surface to deep, branched convexities and folds, although the functional significance of this trait is unclear. As variation in the degree of foliation similarly exists throughout vertebrate evolution, it becomes critical to understand this evolutionary process in a wide variety of species. However, current methods are either qualitative and lack numerical rigor or they are restricted to two dimensions. In this paper, a recently developed method for the characterization of shapes embedded within noisy, three-dimensional data called spherical wave decomposition (SWD) is applied to the problem of characterizing cerebellar foliation in cartilaginous fishes. The SWD method provides a quantitative characterization of shapes in terms of well-defined mathematical functions. An additional feature of the SWD method is the construction of a statistical criterion for the optimal fit, which represents the most parsimonious choice of parameters that fits to the data without overfitting to background noise. We propose that this optimal fit can replace a previously described qualitative visual foliation index (VFI) in cartilaginous fishes with a quantitative analog, i.e. the cerebellar foliation index (CFI). The capability of the SWD method is demonstrated in a series of volumetric images of brains from different chondrichthyan species that span the range of foliation gradings currently described for this group. The CFI is consistent with the qualitative grading provided by the VFI, delivers a robust measure of cerebellar foliation, and can provide a quantitative basis for brain shape characterization across taxa.

The coelacanth rostral organ is a unique low-resolution electro-detector that facilitates the feeding strike.

The cartilaginous and non-neopterygian bony fishes have an electric sense typically comprised of hundreds or thousands of sensory canals distributed in broad clusters over the head. This morphology facilitates neural encoding of local electric field intensity, orientation, and polarity, used for determining the position of nearby prey. The coelacanth rostral organ electric sense, however, is unique in having only three paired sensory canals with distribution restricted to the dorsal snout, raising questions about its function. To address this, we employed magnetic resonance imaging methods to map electrosensory canal morphology in the extant coelacanth, Latimeria chalumnae, and a simple dipole 'rabbit ears' antennae model with toroidal gain function to approximate their directional sensitivity. This identified a unique focal region of electrosensitivity directly in front of the mouth, and is the first evidence of a low-resolution electro-detector that solely facilitates prey ingestion.

Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods.

The polypterids (bichirs and ropefish) are extant basal actinopterygian (ray-finned) fishes that breathe air and share similarities with extant lobe-finned sarcopterygians (lungfishes and tetrapods) in lung structure. They are also similar to some fossil sarcopterygians, including stem tetrapods, in having large paired openings (spiracles) on top of their head. The role of spiracles in polypterid respiration has been unclear, with early reports suggesting that polypterids could inhale air through the spiracles, while later reports have largely dismissed such observations. Here we resolve the 100-year-old mystery by presenting structural, behavioural, video, kinematic and pressure data that show spiracle-mediated aspiration accounts for up to 93% of all air breaths in four species of Polypterus. Similarity in the size and position of polypterid spiracles with those of some stem tetrapods suggests that spiracular air breathing may have been an important respiratory strategy during the fish-tetrapod transition from water to land.

The Digital Fish Library: using MRI to digitize, database, and document the morphological diversity of fish.

Museum fish collections possess a wealth of anatomical and morphological data that are essential for documenting and understanding biodiversity. Obtaining access to specimens for research, however, is not always practical and frequently conflicts with the need to maintain the physical integrity of specimens and the collection as a whole. Non-invasive three-dimensional (3D) digital imaging therefore serves a critical role in facilitating the digitization of these specimens for anatomical and morphological analysis as well as facilitating an efficient method for online storage and sharing of this imaging data. Here we describe the development of the Digital Fish Library (DFL, http://www.digitalfishlibrary.org), an online digital archive of high-resolution, high-contrast, magnetic resonance imaging (MRI) scans of the soft tissue anatomy of an array of fishes preserved in the Marine Vertebrate Collection of Scripps Institution of Oceanography. We have imaged and uploaded MRI data for over 300 marine and freshwater species, developed a data archival and retrieval system with a web-based image analysis and visualization tool, and integrated these into the public DFL website to disseminate data and associated metadata freely over the web. We show that MRI is a rapid and powerful method for accurately depicting the in-situ soft-tissue anatomy of preserved fishes in sufficient detail for large-scale comparative digital morphology. However these 3D volumetric data require a sophisticated computational and archival infrastructure in order to be broadly accessible to researchers and educators.

Evolution of the light organ system in ponyfishes (Teleostei: Leiognathidae).

Members of the leiognathid subfamily Gazzinae, comprising approximately two-thirds of ponyfish species, are sexually dimorphic with regard to features of the light organ system (LOS). In Gazzinae, the circumesophageal light organ (LO) of males is enlarged and varies in shape compared with similarly sized conspecific females. In association with male species-specific translucent external patches on the head and flank, these sexually dimorphic LO features are hypothesized to be correlated with species-specific luminescence displays. Anatomical differences in LO shape, volume, and orientation, and its association with the gas bladder and other internal structures that function in light emission, are compared to observations of luminescence displays for every major lineage within Leiognathidae. We reconstruct the character evolution of both internal and external morphological features of the LOS to investigate the evolution of LO sexual dimorphism and morphology. Both internal and external sexual dimorphism in the ponyfish LOs were recovered as most likely to have evolved in the common ancestor of Leiognathidae, and likelihood-based correlation analyses indicate that the evolution of internal and external dimorphism in males is statistically correlated. Magnetic resonance imaging technology was applied to examine the unique internal LOs of ponyfishes in situ, which provides a new metric (LO index) for comparison of LO structure across lineages.