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Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ.

ABSTRACT: The mechanosensory lateral line, found only in fishes and amphibians, is an important sense organ associated with aquatic life. Lateral line patterns differ among teleost, the most diverse vertebrate taxa, hypothetically in response to selective pressures from different aquatic habitats. In this article, we conduct evolutionary genomic analyses of 34 genes associated with lateral line system development in teleosts to elucidate the significance of contrasting evolutionary rates and changes in the protein coding sequences. We find that duplicated copies of these genes are preferentially retained in the teleost genomes and that episodic events of positive selection have occurred in 22 of the 30 postduplication branches. In general, teleost genes evolved at a faster rate relative to their tetrapod counterparts, and the mutation rates of 26 of the 34 genes differed among teleosts and tetrapods. We conclude that following whole genome duplication, evolutionary rates and episodic events of positive selection on the lateral line system development genes might have been one of the factors favoring the subsequent adaptive radiation of teleosts into diverse habitats. These results provide the foundation for further detailed explorations into lateral line system genes and the evolution of diverse phenotypes and adaptations.

SUBMITTER: Philip S

PROVIDER: S-EPMC3494275 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ.

Philip Siby S Machado João Paulo JP Maldonado Emanuel E Vasconcelos Vítor V O'Brien Stephen J SJ Johnson Warren E WE Antunes Agostinho A

Molecular biology and evolution 20120727 12

The mechanosensory lateral line, found only in fishes and amphibians, is an important sense organ associated with aquatic life. Lateral line patterns differ among teleost, the most diverse vertebrate taxa, hypothetically in response to selective pressures from different aquatic habitats. In this article, we conduct evolutionary genomic analyses of 34 genes associated with lateral line system development in teleosts to elucidate the significance of contrasting evolutionary rates and changes in th ...[more]

PMID: 22844072

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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.

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: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.

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Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ.

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Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ.

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