Indeterminate body growth and lack of gonadal decline in the brown ghost knifefish (Apteronotusleptorhynchus), an organism exhibiting negligible brain senescence

Abstract

The brown ghost knifefish (Apteronotus leptorhynchus (Ellis in Eigenmann, 1912)) is the only vertebrate organism identified thus far that exhibits negligible brain senescence. The present study examines the basic growth patterns of this species, testing the hypothesis that indeterminate growth and lack of reproductive senescence correlate with negligible senescence. Analysis of length-mass relationships revealed negative allometric growth in males and isometric growth in females. Total length at first sexual maturity was 13.5 cm in males and 12.0 cm in females, whereas gonadal mass was 0.02 g in males and 0.2 g in females. Modelling of total length as a function of the number of otolith rings using attenuating growth equations revealed that lengths of up to 26.8 cm in males and 20.2 cm in females can be reached, indicating that the fish continue to grow throughout life. Gonadal mass increased significantly with age in sexually immature individuals of both sexes. In sexually mature fish, gonadal mass showed a marginal increase with age in males and no change in females. The demonstration of indeterminate growth of the fish and of the lack of gonadal regression with age has important implications for the characterization of brown ghost knifefish as a model of negligible senescence.Résumé : Le poisson-couteau brun (Apteronotus leptorhynchus (Ellis in Eigenmann, 1912)) est le seul organisme vertébré identifié à ce jour qui présente une sénescence négligeable du cerveau. L'étude se penche sur les motifs de croissance de base de cette espèce afin de vérifier l'hypothèse voulant que la croissance indéterminée et l'absence de sénescence reproductrice soient corrélées à une sénescence négligeable. L'analyse des relations longueur-masse a révélé une croissance allométrique négative chez les mâles et une croissance isométrique chez les femelles. La longueur totale à l'atteinte de la maturité sexuelle était de 13,5 cm pour les mâles et de 12,0 cm pour les femelles, alors que la masse des gonades était de 0,02 g pour les mâles et de 0,2 g pour les femelles. La modélisation de la longueur totale en fonction du nombre d'anneaux d'otolithe à l'aide d'équations d'atténuation de la croissance a révélé que des longueurs de jusqu'à 26,8 cm pour les mâles et 20,2 cm pour les femelles peuvent être atteintes, ce qui indique que les poissons continuent de croître tout au long de leur vie. La masse des gonades augmentait de manière significative avec l'âge chez les individus sexuellement immatures des deux sexes. Chez les poissons sexuellement matures, la masse des gonades présentait une augmentation marginale avec l'âge chez les mâles et aucun changement chez les femelles. La démonstration de la croissance indéterminée de ces poissons et l'absence de régression des gonades avec l'âge ont d'importantes conséquences en ce qui concerne la caractérisation du poisson-couteau brun en tant que modèle de sénescence négligeable. [Traduit par la Rédaction]Mots-clés : neurogénèse adulte, Apteronotus leptorhynchus, poisson-couteau brun, croissance ...

Additive neurogenesis supported by multiple stem cell populations mediates adult spinal cord development: A spatiotemporal statistical mapping analysis in a teleost model of indeterminate growth

“…The teleost fish A. leptorhynchus is distinguished by its ability to generate new neurons in its brain and spinal cord throughout adulthood (for reviews, see Sîrbulescu and Zupanc, ; Zupanc and Sîrbulescu, ; Sîrbulescu and Zupanc, ; Zupanc and Sîrbulescu, ; Zupanc, ). This continued neurogenesis parallels, and is probably driven by, the indeterminate growth of the fish (Ilieş et al, ). Using this species as one of the best‐characterized teleostean model systems of adult neurogenesis, this study provides the first comprehensive quantitative analysis of tissue growth mediated by continued cellular proliferation in the adult CNS of any vertebrate.…”

“…The gonadosomatic index (defined as the ratio between gonadal weight and body weight) averaged 0.27% (SD: 0.11%) in males and 3.04% (SD: 2.32%) in females. These data indicate that all fish were adults in their second or third year of life (Ilieş et al, ). All animal experiments were approved by the Institutional Animal Care and Use Committee of Northeastern University.…”

“…Combined with low levels of apoptotic cell death in the intact spinal cord (Sîrbulescu et al, ), the persistent cell proliferation and differentiation lead to a continuous addition of new cells. As a consequence, the spinal cord of this teleost fish continues to grow during adulthood, paralleling the indeterminate growth of the fish (Ilieş et al, ). Assuming that the rostral trend levels of the various linear densities do not increase over time because of the continuous proliferation, our model predicts that cell counts will grow proportionally to the fish's spinal cord length.…”

“…In addition, A. leptorhynchus is distinguished by the lack of any significant age‐related decline in the proliferation of adult stem cells in the brain, in neuronal or glial differentiation, or in the long‐term survival of the newly generated cells (Traniello et al, ). This persistent neurogenic activity, combined with limited cell death and long‐term survival of the new cells (Soutschek and Zupanc, ; Ott et al, ), leads to continuous growth of the adult brain, in concert with the continued growth of the fish (Ilieş et al, ). Quantitative analysis has shown that, as in the spinal cord, the total number of brain cells doubles from ∼50 to 100 million during the growth of adult individuals of A. leptorhynchus from 100 to 200 mm in length (Zupanc and Horschke, ).…”

“…Our current data and model suggest that fish of the size ranges examined (∼150 mm total length, indicating that the fish were 2–3 years old) harbor a total of about 18,900 electromotor neurons in their spinal cord. By the time a fish reaches a total length of 160 mm, which takes approximately 100 days (Ilieş et al, ), an estimated 1,260 new electromotor neurons are added, corresponding to a 7% increase relative to a 150‐mm‐long fish.…”