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Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

ABSTRACT: BACKGROUND: The canals of the mechanosensory lateral line system are components of the dermatocranium, and demonstrate phenotypic variation in bony fishes. Widened lateral line canals evolved convergently in a limited number of families of teleost fishes and it had been hypothesized that they evolved from narrow canals via heterochrony and explore modularity in the lateral line system. Two species of cichlids with different canal phenotypes were used to test a hypothesis of heterochrony. Histological material prepared from ontogenetic series of Aulonocara stuartgranti (widened canals) and Tramitichromis sp. (narrow canals) was analyzed using ANCOVA to determine rates of increase in canal diameter and neuromast size (length, width) and to compare the timing of onset of critical stages in canal morphogenesis (enclosure, ossification). RESULTS: A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis. However, rates of increase in canal diameter and neuromast size among canals, among canal portions and among canals segments reveal similar trends within both species. CONCLUSION: The evolution of widened lateral line canals is the result of dissociated heterochrony - acceleration in the rate of increase of both canal diameter and neuromast size, and delay in the onset of canal morphogenesis, in Aulonocara (widened canals) relative to Tramitichromis (narrow canals). Common rates of increase in canal diameter and neuromast size among canal portions in different dermatocranial bones and among canal segments reflect the absence of local heterochronies, and suggest modular integration among canals in each species. Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found. Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences. Heterochrony can likely explain the convergent evolution of widened lateral line canals among diverse taxa. The lateral line system provides a valuable context for novel analyses of the relationship between developmental processes and the evolution of behaviorally and ecologically relevant phenotypes in fishes.

SUBMITTER: Bird NC

PROVIDER: S-EPMC4066827 | biostudies-other | 2014

REPOSITORIES: biostudies-other

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Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

Bird Nathan C NC Webb Jacqueline F JF

EvoDevo 20140605

<h4>Background</h4>The canals of the mechanosensory lateral line system are components of the dermatocranium, and demonstrate phenotypic variation in bony fishes. Widened lateral line canals evolved convergently in a limited number of families of teleost fishes and it had been hypothesized that they evolved from narrow canals via heterochrony and explore modularity in the lateral line system. Two species of cichlids with different canal phenotypes were used to test a hypothesis of heterochrony. ...[more]

PMID: 24959342

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Project description:Animals use multiple senses during social interactions and must integrate this information in the brain to make context-dependent behavioral decisions. For fishes, the largest group of vertebrates, the mechanosensory lateral line system provides crucial hydrodynamic information for survival behaviors, but little is known about its function in social communication. Our previous work using the African cichlid fish, Astatotilapia burtoni, provided the first empirical evidence that fish use their lateral line system to detect water movements from conspecifics for mutual assessment and behavioral choices. It is unknown, however, where this socially-relevant mechanosensory information is processed in the brain to elicit adaptive behavioral responses. To examine for the first time in any fish species which brain regions receive contextual mechanosensory information, we quantified expression of the immediate early gene cfos as a proxy for neural activation in sensory and socially-relevant brain nuclei from lateral line-intact and -ablated fish following territorial interactions. Our in situ hybridization results indicate that in addition to known lateral line processing regions, socially-relevant mechanosensory information is processed in the ATn (ventromedial hypothalamus homolog), Dl (putative hippocampus homolog), and Vs (putative medial extended amygdala homolog). In addition, we identified a functional network within the conserved social decision-making network (SDMN) whose co-activity corresponds with mutual assessment and behavioral choice. Lateral line-intact and -ablated fight winners had different patterns of co-activity of these function networks and group identity could be determined solely by activation patterns, indicating the importance of mechanoreception to co-activity of the SDMN. These data show for the first time that the mechanosensory lateral line system provides relevant information to conserved decision-making centers of the brain during territorial interactions to mediate crucial behavioral choices such as whether or not to engage in a territorial fight. To our knowledge, this is also the first evidence of a subpallial nucleus receiving mechanosensory input, providing important information for elucidating homologies of decision-making circuits across vertebrates. These novel results highlight the importance of considering multimodal sensory input in mediating context-appropriate behaviors that will provide broad insights on the evolution of decision-making networks across all taxa.

Project description:Fishes use multimodal signals during both inter- and intra-sexual displays to convey information about their sex, reproductive state, and social status. These complex behavioral displays can include visual, auditory, olfactory, tactile, and hydrodynamic signals, and the relative role of each sensory channel in these complex multi-sensory interactions is a common focus of neuroethology. The mechanosensory lateral line system of fishes detects near-body water movements and is implicated in a variety of behaviors including schooling, rheotaxis, social communication, and prey detection. Cobalt chloride is commonly used to chemically ablate lateral line neuromasts, thereby eliminating water-movement cues to test for mechanosensory-mediated behavioral functions. However, cobalt acts as a nonspecific calcium channel antagonist and could potentially disrupt function of all superficially located sensory receptor cells, including those for chemosensing. Here, we examined whether CoCl2 treatment used to ablate the lateral line system also impairs olfaction in three freshwater fishes, the African cichlid fish Astatotilapia burtoni, goldfish Carassius auratus, and the Mexican blind cavefish Astyanax mexicanus. To examine the impact of CoCl2 on the activity of peripheral receptors, we quantified DASPEI fluorescence intensity of the olfactory epithelium from fish exposed to control and CoCl2 solutions. In addition, we examined brain activation in olfactory processing regions of A. burtoni immersed in either control or cobalt solutions. All three species exposed to CoCl2 had decreased DASPEI staining of the olfactory epithelium, and in A. burtoni, cobalt treatment caused reduced neural activation in olfactory processing regions of the brain. To our knowledge this is the first empirical evidence demonstrating that the same CoCl2 treatment used to ablate the lateral line system also impairs olfactory function. These data have important implications for the use of CoCl2 in future research and suggest that previous studies using CoCl2 should be reinterpreted in the context of both impaired mechanoreception and olfaction.

Project description:In humans, the absence or irreversible loss of hair cells, the sensory mechanoreceptors in the cochlea, accounts for a large majority of acquired and congenital hearing disorders. In the auditory and vestibular neuroepithelia of the inner ear, hair cells are accompanied by another cell type called supporting cells. This second cell population has been described as having stem cell-like properties, allowing efficient hair cell replacement during embryonic and larval/fetal development of all vertebrates. However, mammals lose their regenerative capacity in most inner ear neuroepithelia in postnatal life. Remarkably, reptiles, birds, amphibians, and fish are different in that they can regenerate hair cells throughout their lifespan. The lateral line in amphibians and in fish is an additional sensory organ, which is used to detect water movements and is comprised of neuroepithelial patches, called neuromasts. These are similar in ultra-structure to the inner ear's neuroepithelia and they share the expression of various molecular markers. We examined the regeneration process in hair cells of the lateral line of zebrafish larvae carrying a retroviral integration in a previously uncharacterized gene, phoenix (pho). Phoenix mutant larvae develop normally and display a morphologically intact lateral line. However, after ablation of hair cells with copper or neomycin, their regeneration in pho mutants is severely impaired. We show that proliferation in the supporting cells is strongly decreased after damage to hair cells and correlates with the reduction of newly formed hair cells in the regenerating phoenix mutant neuromasts. The retroviral integration linked to the phenotype is in a novel gene with no known homologs showing high expression in neuromast supporting cells. Whereas its role during early development of the lateral line remains to be addressed, in later larval stages phoenix defines a new class of proteins implicated in hair cell regeneration.

Dataset Information

Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

Publications

Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

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