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Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis.

ABSTRACT: Very few studies have described brain scaling in vertebrates throughout ontogeny and none in lampreys, one of the two surviving groups of the early agnathan (jawless) stage in vertebrate evolution. The life cycle of anadromous parasitic lampreys comprises two divergent trophic phases, firstly filter-feeding as larvae in freshwater and secondly parasitism as adults in the sea, with the transition marked by a radical metamorphosis. We characterized the growth of the brain during the life cycle of the pouched lamprey Geotria australis, an anadromous parasitic lamprey, focusing on the scaling between brain and body during ontogeny and testing the hypothesis that the vast transitions in behavior and environment are reflected in differences in the scaling and relative size of the major brain subdivisions throughout life. The body and brain mass and the volume of six brain structures of G. australis, representing six points of the life cycle, were recorded, ranging from the early larval stage to the final stage of spawning and death. Brain mass does not increase linearly with body mass during the ontogeny of G. australis. During metamorphosis, brain mass increases markedly, even though the body mass does not increase, reflecting an overall growth of the brain, with particularly large increases in the volume of the optic tectum and other visual areas of the brain and, to a lesser extent, the olfactory bulbs. These results are consistent with the conclusions that ammocoetes rely predominantly on non-visual and chemosensory signals, while adults rely on both visual and olfactory cues.

SUBMITTER: Salas CA

PROVIDER: S-EPMC4517384 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis.

Salas Carlos A CA Yopak Kara E KE Warrington Rachael E RE Hart Nathan S NS Potter Ian C IC Collin Shaun P SP

Frontiers in neuroscience 20150728

Very few studies have described brain scaling in vertebrates throughout ontogeny and none in lampreys, one of the two surviving groups of the early agnathan (jawless) stage in vertebrate evolution. The life cycle of anadromous parasitic lampreys comprises two divergent trophic phases, firstly filter-feeding as larvae in freshwater and secondly parasitism as adults in the sea, with the transition marked by a radical metamorphosis. We characterized the growth of the brain during the life cycle of ...[more]

PMID: 26283894

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Project description:Background and aimsSimple models of herbaceous plant growth based on optimal partitioning theory predict, at steady state, an isometric relationship between shoot and root biomass during plant ontogeny, i.e. a constant root-shoot ratio. This prediction has received mixed empirical support, suggesting either that optimal partitioning is too coarse an assumption to model plant biomass allocation, or that additional processes need to be modelled to account for empirical findings within the optimal partitioning framework. In this study, simulations are used to compare quantitatively two potential explanations for observed non-isometric relationships, namely nutrient limitation during the experiments and initial developmental constraints.MethodsA simple plant growth model was built to simulate the growth of herbaceous species, based on optimal partitioning theory combined with empirically measured plant functional traits. Its ability to reproduce plant relative growth rate and final root weight ratio was assessed against previously published data. Predicted root-shoot ratios during plant ontogeny were compared with experimental observations. The effects of nutrient limitation and initial developmental constraints on root-shoot ratios were then tested.Key resultsThe model was found to reproduce overall plant growth patterns accurately, but failed, in its simplest form, at explaining non-isometric growth trajectories. Both nutrient limitation and ontogenetic developmental constraints were further shown to cause transient dynamics resulting in a deviation from isometry. Nitrogen limitation alone was not sufficient to explain the observed trajectories of most plant species. The inclusion of initial developmental constraints (fixed non-optimal initial root-shoot ratios) enabled the reproduction of the observed trajectories and were consistent with observed initial root-shoot ratios.ConclusionsThis study highlights the fact that considering transient dynamics enables theoretical predictions based on optimal partitioning to be reconciled with empirically measured ontogenetic root-shoot allometries. The transient dynamics cannot be solely explained by nutrient limitation during the experiments, pointing to a likely role for initial developmental constraints in the observed non-isometric growth trajectories.

Project description:BACKGROUND:The Argentinian pouched lamprey, classified as Petromyzon macrostomus Burmeister, 1868 was first described in 1867 in De La Plata River, in Buenos Aires, Argentina, and subsequently recorded in several rivers from Patagonia. Since its original description, the validity of P. macrostomus was questioned by several ichthyologists and 36 years after its original discovery it was considered a junior synonym of Geotria australis Gray, 1851. For a long time, the taxonomic status of G. australis has been uncertain, largely due to the misinterpretations of the morphological alterations that occur during sexual maturation, including the arrangement of teeth, size and position of fins and cloaca, and the development of an exceptionally large gular pouch in males. In this study, the taxonomic status of Geotria from across the "species" range was evaluated using both molecular analysis and examination of morphological characteristics. METHODOLOGY/PRINCIPAL FINDINGS:Phylogenetic and species delimitation analyses based on mitochondrial DNA sequences of Cytochrome b (Cyt b) and Cytochrome C Oxidase Subunit 1 (COI) genes, along with morphological analysis of diagnostic characters reported in the original descriptions of the species were used to assess genetic and morphological variation within Geotria and to determine the specific status of the Argentinian lamprey. These analyses revealed that Geotria from Argentina constitutes a well differentiated lineage from Chilean and Australasian populations. The position of the cloaca and the distance between the second dorsal and caudal fins in sub-adult individuals, and at previous life stages, can be used to distinguish between the two species. In addition, the genetic distance between G. macrostoma and G. australis for the COI and Cyt b mitochondrial genes is higher than both intra- and inter-specific distances reported for other Petromyzontiformes. CONCLUSIONS/SIGNIFICANCE:Our results indicate that the Argentinian pouched lamprey, found along a broad latitudinal gradient on the south-west Atlantic coast of South America, should be named as Geotria macrostoma (Burmeister, 1868) and not as G. australis Gray 1851, returning to its earliest valid designation in Argentina. Geotria macrostoma can now be considered as the single lamprey species inhabiting Argentinian Patagonia, with distinct local adaptations and evolutionary potential. It is essential that this distinctiveness is recognized in order to guide future conservation and management actions against imminent threats posed by human actions in the major basins of Patagonia.

Project description:Lampreys are one of the two surviving groups of the agnathan (jawless) stages in vertebrate evolution and are thus ideal candidates for elucidating the evolution of visual systems. This study investigated the retinal amino acid neurochemistry of the southern hemisphere lamprey Geotria australis during the downstream migration of the young, recently-metamorphosed juveniles to the sea and during the upstream migration of the fully-grown and sexually-maturing adults to their spawning areas. Glutamate and taurine were distributed throughout the retina, whilst GABA and glycine were confined to neurons of the inner retina matching patterns seen in most other vertebrates. Glutamine and aspartate immunoreactivity was closely matched to Müller cell morphology. Between the migratory phases, few differences were observed in the distribution of major neurotransmitters i.e. glutamate, GABA and glycine, but changes in amino acids associated with retinal metabolism i.e. glutamine and aspartate, were evident. Taurine immunoreactivity was mostly conserved between migrant stages, consistent with its role in primary cell functions such as osmoregulation. Further investigation of glutamate signalling using the probe agmatine (AGB) to map cation channel permeability revealed entry of AGB into photoreceptors and horizontal cells followed by accumulation in inner retinal neurons. Similarities in AGB profiles between upstream and downstream migrant of G. australis confirmed the conservation of glutamate neurotransmission. Finally, calcium binding proteins, calbindin and calretinin were localized to the inner retina whilst recoverin was localized to photoreceptors. Overall, conservation of major amino acid neurotransmitters and calcium-associated proteins in the lamprey retina confirms these elements as essential features of the vertebrate visual system. On the other hand, metabolic elements of the retina such as neurotransmitter precursor amino acids and Müller cells are more sensitive to environmental changes associated with migration.

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Dataset Information

Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis.

Publications

Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis.

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