We study the structural and functional development and evolution of fish sensory systems. Our work is focused on the mechanosensory lateral line system, a primitive vertebrate sensory system found in all 30,000+ fishes (and larval and aquatic adult amphibians) – and thus in more than half of the vertebrate species on earth. The lateral line system detects water flows facilitating prey detection, predator avoidance, communication, and navigation (including rheotaxis). Furthermore, unlike the nose, eyes and ears, which are found on the head of all vertebrates, the lateral line system is composed of many small sense organs (neuromasts) found on the skin and in pored canals, which in bony fishes are found within a conserved subset of skull bones on the head and in the trunk canal contained within lateral line scales on the body.
Thus, the lateral line system has a dual identity – as an essential sensory system that mediates critical behaviors, and as a component of the skull of bony fishes. The role of the lateral line system in behavior will shed light on how fishes may overcome challenges presented by global change, such as reduced water clarity, which likely requires increased dependence on non-visual sensory systems for prey detection, predator avoidance, navigation, and communication. Furthermore, the study of the system contributes to our understanding of sensory biology, evolutionary developmental biology, and development and evolution of the vertebrate skull.
We have studied the lateral line system in a wide range of taxa including: flounders, greenlings, zebrafish, skates, coral reef butterflyfishes and gobies, Lake Malawi cichlids, and deep-sea (stomiiform) fishes. Each group has interesting or unique attributes that have allowed us to ask fundamental questions about lateral line evolution, development, functional morphology, and the sensory basis for behavior.We have used multiple methods including histology, SEM, CT/µCT, vital fluorescent imaging, and fate mapping to gain a comprehensive understanding of patterns of lateral line morphology and development. We have also used DPIV (for analysis of hydrodynamic stimuli), video analysis of behavior, and classical fish training (conditioned responses to artificial hydrodynamic stimuli) to study the sensory basis for feeding behavior under different environmental conditions.
Our work has been funded by the National Science Foundation, a NSF Graduate Research Fellowship, the Lerner Gray Fund of the American Museum of Natural History, the Marine Biological Laboratory (Woods Hole), RI NSF EPSCoR, and the University of Rhode Island.
Sensory Biology of Coral Reef Fishes
Coral reef fishes are speciose and taxonomically diverse, although the majority of species are percomorph (“higher” teleost) fishes. They live in relatively shallow, well-lit waters and are considered to be visually oriented. However, our understanding of sensory integration in fishes, more generally, demands that we also consider the non-visual senses and their roles in diverse behaviors. Our work has focused on the morphology and development of the lateral line system in major groups of coral reef fishes – the gobies, butterflyfishes, damselfishes, wrasses, and parrotfishes.
- The Role of Larval Orientation Behavior in Determining Population Connectivity – Sensory Ontogeny in a Coral Reef Goby (ongoing). Most coral reef fishes (and most marine fishes) have a complex life history that includes the dispersal of planktonic eggs and pelagic larvae, with remarkable swimming abilities. Late stage larvae of coral reef fishes are known to respond to olfactory, auditory, and visual cues to change their behavior and navigate to their settlement sites on reefs, but the morphology and development of the sensory systems that underlie these behaviors are not well studied. In this collaborative project with colleagues at Boston University and University of Miami, we are using a goby (Elactinus lori) for the first integrated analysis of the ontogeny of multiple sensory systems (olfaction, taste, lateral line, hearing, vision) and larval orientation behavior in a coral reef fish. The ultimate goal is to understand how the different sensory systems and navigation behavior contribute to settlement patterns, and thus population connectivity. Funded by NSF grant 1459546 (Ocean Sciences). See: Goby Sensory Ontogeny page.
- The Laterophysic Connection in Butterflyfishes – The swim bladders of a diversity of teleost fishes have convergently evolved associations with the inner ear (otophysic connections) that enhance the reception of sound. We have described the comparative anatomy, development, and systematic significance of the laterophysic connection, a unique swim bladder-lateral line linkage in butterflyfishes in the genus Chaetodon, which is hypothesized to enhance the ability of the lateral line system to respond to acoustic stimuli in the context of critical behaviors, including territoriality and monogamous social systems. Tricas and Webb (2016) reviews this work as well as the behavioral and physiological work on sound production and sound reception carried out by the Tricas lab. Funded by NSF grants IBN 9603896 and IBN 0132607. See: Butterflyfish Project page.
- The Lateral Line System of Damselfishes, Wrasses, and Parrotfishes – As part of her PhD dissertation (1988), Dr. Webb examined the diversity and evolution of patterns (complete, incomplete, disjunct) of the trunk canal with respect to body shape and morphology of the lateral line scales (see Webb, 1990, in Copeia).
Flow Sensing in the Deep Sea: The Lateral Line System of Stomiiform Fishes
The deep sea is a hydrodynamically quiet environment characterized by low light levels or complete darkness, in which the evolution of both the visual and the non-visual senses should be favored. Several groups of mesopelagic and bathypelagic fishes are known to have specializations of the lateral line system, but little is known about the most speciose order of deep-sea fishes – the hatchetfishes, bristlemouths, and barbelled dragonfishes of the Order Stomiiformes. The morphology of the lateral line system in stomatiiform fishes was investigated for the first time using a range of morphological methods including histology, SEM, and µCT imaging. Results revealed a dramatic enhancement of the lateral line system that had gone unnoticed until now. Funded by an NSF Graduate Research Fellowship, Lerner-Gray Fund for Marine Research Grant (ANMH, NY), and URI. (A. Marranzino, MS Thesis 2016). See: Deep-Sea Lateral Line page.
Cichlid Fishes: Development and Evolution of the Mechanosensory Lateral Line System
- Phenotypic Evolution in the Lateral Line System of Cichlid Fishes. Representatives of two genera of Lake Malawi (Africa) cichlid fishes (Aulonocara [widened canals] and Tramitichromis [narrow canals]) are being used for comparative anatomical, developmental, and behavioral studies that address fundamental issues in post-embryonic lateral line development, diversification of lateral line phenotypes, and functional evolution of the lateral line system of fishes (Becker, MS Thesis; Carter, MS Thesis). Funded by NSF grant IOS 0843307. See: Cichlid Project page.
- Dermal Bone Remodeling and Lateral Line Canal Morphogenesis – We are interested in understanding how developmental processes contribute to patterns of lateral line canal morphogenesis, growth, and evolution of the cranial lateral line canals in bony fishes. We seek to determine: a) how lateral line canals become integrated into the dermatocranial bones in bony fishes, and b) how patterns of bone remodeling defines lateral line canal phenotypes (Johnstone, ongoing MS thesis). Funded by URI.
Lateral Line Development in Elasmobranch Fishes
We have studied the development of the lateral line canal system in the little skate, Leucoraja erinacea. In contrast to the bony fishes, the cranial lateral line canals in elasmobranch fishes are not associated bone, but are contained in the soft tissue of the dermis surrounding the elements that compose the cartilaginous skull of these fishes. Furthermore, the pattern of development of the lateral line system in elasmobranchs contrasts with that in bony fishes in fundamental ways. The study of this contrast will shed light on how lateral line development evolved with the divergence of the cartilaginous (elasmobranch) and bony fishes hundreds of millions of years ago. This work has been carried out at the Marine Biological Laboratory (Woods Hole) in collaboration with Dr. Andrew Gillis (Cambridge University, UK). Funded by a Laura and Arthur Colwin Endowed Summer Research Fellowship at the MBL and the University of Rhode Island. See: Skate Project page.
Imaging of the Cranial Lateral Line Canal System with µCT – We are continuing to develop methods for visualizing and quantifying the morphology of the cranial lateral line canals of teleost fishes in both 2D and 3D. See: µCT Imaging Page.
Photo credit: Dr. Margot Schwalbe