Comparison of captive lifespan, age-associated liver neoplasias and age-dependent gene expression between two annual fish species: Nothobranchius furzeri and Nothobranchius korthause

Baumgart, Mario; Cicco, Emiliano Di; Rossi, Giacomo; Cellerino, Alessandro; Tozzini, Eva Terzibasi

doi:10.1007/s10522-014-9535-y

Cited by 24 publications

(23 citation statements)

References 23 publications

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“…A). N. korthausae shows similar macroscopic age phenotypes as N. furzeri , although their onset is delayed, as this species can survive for up to 18 months (Lucas‐Sánchez et al, ; Baumgart et al, ). Remarkably, the expression of these age‐dependent phenotypes is rather variable across individuals of the same age; some individuals displaying the ‘decrepit’ phenotype may survive for months.…”

Section: The Ageing Phenotypementioning

confidence: 97%

“…They have a short maximum natural lifespan (<12 months) due to annual desiccation of the pools in which they live. Notably, this short lifespan is also retained in captivity, varying between 3 and 18 months (Valdesalici & Cellerino, 2003;Lucas-Sánchez et al, 2011;Baumgart et al, 2015). The Nothobranchius life cycle is entirely adapted to the ephemeral and unpredictable conditions of their habitat.…”

Section: Introductionmentioning

confidence: 99%

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From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology

2015

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African annual fishes from the genus Nothobranchius are small teleosts that inhabit temporary water bodies subject to annual desiccation due to the alternation of the monsoon seasons. Given their unique biology, these fish have emerged as a model taxon in several biological disciplines. Their increasing popularity stems from the extremely short lifespan that is the result of their specific life-history adaptations and is retained under laboratory conditions. Nothobranchius furzeri, the most popular laboratory species, is the vertebrate species with the shortest lifespan recorded in captivity. In the laboratory, adults of different Nothobranchius species and populations live between 3 and 18 months and, notably, there is a negative correlation between the captive lifespan of a species and the aridity of their habitat. Their short lifespan is coupled to rapid age-dependent functional decline and expression of cellular and molecular changes comparable to those observed in other vertebrates, including humans. The recent development of transgenesis in this species makes it possible to insert specific constructs into their genome, and the establishment of transgenic lines is facilitated by their very rapid generation time, which can be as short as 1 month. This makes Nothobranchius species particularly suited for investigating biological and molecular aspects of ageing and ageing-associated dysfunctions. At the same time, they also represent a unique model taxon to investigate the evolution of life-history adaptations and their genetic architecture. We review their natural history, including phylogenetic relationships, distribution in relation to habitat conditions and natural selection for differential longevity, population structure and demography, and life cycle with emphasis on diapause that may occur at three stages during embryonic development. We further critically evaluate their use as a laboratory model for understanding the evolution of a rapid ageing rate and its consequences for other life-history traits, for cellular, molecular and integrative traits associated with the ageing process, high incidence of neoplasias, their utility for genome-wide gene-expression studies, and as a model for quantitative genetics. We summarize recent achievements in fostering Nothobranchius species as a widely applicable model system, including an annotated transcriptome, successful transgenesis, and existence of viable inbred lines. We compare the conditions they experience in the wild and in captivity and suggest that they are an ideal taxon to investigate natural genetic variation in a laboratory setting. We conclude that Nothobranchius species -and N. furzeri in particular -could become a unique model taxon that bridges interests in ecological and biomedical research. We hope that a conceptual and methodological integration of these two branches of biology will provide important new insights.

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Section: The Ageing Phenotypementioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology

2015

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“…; Baumgart et al. ). Decrease in reproductive success is another important source of decline in individual fitness contributing to aging, with recognized differences among species (Bouwhuis et al.…”

Section: Overview Of Study Populations and Their Originmentioning

confidence: 98%

“…Lower RONS formation and/or higher resistance of cellular components to oxidative damage correlates with elevated longevity (Monaghan et al 2009;Pamplona and Costantini 2011). Neoplasia represent a serious functional decline associated with aging in vertebrates, including fishes (Kishi et al 2003), and is associated with other functional declines (di Cicco et al 2011;Baumgart et al 2015). Decrease in reproductive success is another important source of decline in individual fitness contributing to aging, with recognized differences among species (Bouwhuis et al 2012;Jones et al 2008) and the potential for variation among populations of a species.…”

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confidence: 99%

Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient

et al. 2016

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Life span and aging are substantially modified by natural selection. Across species, higher extrinsic (environmentally related) mortality (and hence shorter life expectancy) selects for the evolution of more rapid aging. However, among populations within species, high extrinsic mortality can lead to extended life span and slower aging as a consequence of condition-dependent survival. Using within-species contrasts of eight natural populations of Nothobranchius fishes in common garden experiments, we demonstrate that populations originating from dry regions (with short life expectancy) had shorter intrinsic life spans and a greater increase in mortality with age, more pronounced cellular and physiological deterioration (oxidative damage, tumor load), and a faster decline in fertility than populations from wetter regions. This parallel intraspecific divergence in life span and aging was not associated with divergence in early life history (rapid growth, maturation) or pace-of-life syndrome (high metabolic rates, active behavior). Variability across four study species suggests that a combination of different aging and life-history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in life span and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly.

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“…We previously sequenced and assembled the genome of N. furzeri as well as the transcriptomes of N. kadleci (the sister species of N. furzeri ), N. pienaari , N. rachovii , and N. kuhntae together with N. korthause [a long‐lived Nothobranchius , lifespan 18 months (Baumgart et al ., )], and Aphyosemion striatum (lifespan > 3 years) as a representative of the non‐annual sister genus (Reichwald et al ., ). We found seven genes under positive selection in N. furzeri and one in N. pienaari , another very‐short‐lived species, using the other six species of Nothobranchiidae as outgroups (Reichwald et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes

et al. 2017

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SummaryThe current molecular understanding of the aging process derives almost exclusively from the study of random or targeted single‐gene mutations in highly inbred laboratory species, mostly invertebrates. Little information is available as to the genetic mechanisms responsible for natural lifespan variation and the evolution of lifespan, especially in vertebrates. Here, we investigated the pattern of positive selection in annual (i.e., short‐lived) and nonannual (i.e., longer‐lived) African killifishes to identify a genomic substrate for evolution of annual life history (and reduced lifespan). We identified genes under positive selection in all steps of mitochondrial biogenesis: mitochondrial (mt) DNA replication, transcription from mt promoters, processing and stabilization of mt RNAs, mt translation, assembly of respiratory chain complexes, and electron transport chain. Signs of paralleled evolution (i.e., evolution in more than one branch of Nothobranchius phylogeny) are observed in four out of five steps. Moreover, some genes under positive selection in Nothobranchius are under positive selection also in long‐lived mammals such as bats and mole‐rats. Complexes of the respiratory chain are formed in a coordinates multistep process where nuclearly and mitochondrially encoded components are assembled and inserted into the inner mitochondrial membrane. The coordination of this process is named mitonuclear balance, and experimental manipulations of mitonuclear balance can increase longevity of laboratory species. Our data strongly indicate that these genes are also casually linked to evolution lifespan in vertebrates.

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Comparison of captive lifespan, age-associated liver neoplasias and age-dependent gene expression between two annual fish species: Nothobranchius furzeri and Nothobranchius korthause

Cited by 24 publications

References 23 publications

From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology

From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology

Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient

Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes

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