Mapping Loci Associated With Tail Color and Sex Determination in the Short-Lived Fish Nothobranchius furzeri

Department of Genetics, Stanford University, Stanford, California 94305, USA.
Genetics (Impact Factor: 5.96). 09/2009; 183(4):1385-95. DOI: 10.1534/genetics.109.108670
Source: PubMed


The African fish Nothobranchius furzeri is the shortest-lived vertebrate species that can reproduce in captivity, with a median life span of 9-11 weeks for the shortest-lived strain. Natural populations of N. furzeri display differences in life span, aging biomarkers, behavior, and color, which make N. furzeri a unique vertebrate system for studying the genetic basis of these traits. We mapped regions of the genome involved in sex determination and tail color by genotyping microsatellite markers in the F(2) progeny of a cross between a short-lived, yellow-tailed strain and a long-lived, red-tailed strain of N. furzeri. We identified one region linked with the yellow/red tail color that maps close to melanocortin 1 receptor (mc1r), a gene involved in pigmentation in several vertebrate species. Analysis of the segregation of sex-linked markers revealed that N. furzeri has a genetic sex determination system with males as the heterogametic sex and markedly reduced recombination in the male sex-determining region. Our results demonstrate that both naturally-evolved pigmentation differences and sex determination in N. furzeri are controlled by simple genetic mechanisms and set the stage for the molecular genetic dissection of factors underlying such traits. The microsatellite-based linkage map we developed for N. furzeri will also facilitate analysis of the genetic architecture of traits that characterize this group of vertebrates, including short life span and adaptation to extreme environmental conditions.

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    • "Because the GRZ strain is highly inbred, we expected genomic variations predominantly in the region of suppressed recombination between male and female sex chromosomes. Accordingly, male single nucleotide variations (SNVs) were mainly confined to a region on sgr05 (Figures 2B and S3A) that bears the only four sex-linked markers identified so far (Kirschner et al., 2012; Valenzano et al., 2009). This male-specific region of the Y chromosome (MSY) encompasses 26.1 Mb (sgr05: 15,031,832–41,162,746) and exhibits a distinct peak in variation density at position 37.6 Mb. "
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    ABSTRACT: The killifish Nothobranchius furzeri is the shortest-lived vertebrate that can be bred in the laboratory. Its rapid growth, early sexual maturation, fast aging, and arrested embryonic development (diapause) make it an attractive model organism in biomedical research. Here, we report a draft sequence of its genome that allowed us to uncover an intra-species Y chromosome polymorphism representing-in real time-different stages of sex chromosome formation that display features of early mammalian XY evolution "in action." Our data suggest that gdf6Y, encoding a TGF-beta family growth factor, is the master sex-determining gene in N. furzeri. Moreover, we observed genomic clustering of aging-related genes, identified genes under positive selection, and revealed significant similarities of gene expression profiles between diapause and aging, particularly for genes controlling cell cycle and translation. The annotated genome sequence is provided as an online resource (
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    • "This is the strain that the large majority of laboratories use for experimental work, and currently is the shortest lived. Based on results obtained from genotyping with microsatellite markers, this strain is highly inbred, with females completely inbred (100% homozygosity in 152 tested microsatellite markers) and males heterozygous exclusively at the sex-linked markers (Valenzano et al., 2009). The genetic homogeneity of the GRZ strain was further confirmed by analysis of single-nucleotide variations (Reichwald et al., 2009; Kirschner et al., 2012). "
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    ABSTRACT: 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. © 2015 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
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    • "Mature F2 generation male and female N. furzeri were maintained in 40 gallon stock tanks in a fish room (25 degrees C, 12 hours light: 12 hours dark daily cycle) and provided with spawning substrate. Eggs were collected daily, over a one month period, and distributed individually into the wells of 48-well tissue culture plates containing Yamamoto's embryo incubation medium (Valenzano et al. 2009). Eggs were incubated at three temperatures (20, 25, and 30°C) crossed with four light treatments (hours light: hours dark—0:24, 10:14, 12:12, 14:10) for a total of 12 different combinations. "
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    ABSTRACT: Two ways in which organisms adapt to variable environments are phenotypic plasticity and bet-hedging. Theory suggests that bet-hedging is expected to evolve in unpredictable environments for which reliable cues indicative of future conditions (or season length) are lacking. Alternatively, if reliable cues exist indicating future conditions, organisms will be under selection to produce the most appropriate phenotype - that is, adaptive phenotypic plasticity. Here we experimentally test which of these modes of adaptation are at play in killifish that have evolved an annual life cycle. These fish persist in ephemeral pools that completely dry each season through the production of eggs that can remain in developmental arrest, or diapause, buried in the soil, until the following rainy season. Consistent with diversified bet-hedging (a risk spreading strategy), we demonstrate that the eggs of the annual killifish Nothobranchius furzeri exhibit variation at multiple levels - whether or not different stages of diapause are entered, for how long diapause is entered, and the timing of hatching - and this variation persists after controlling for both genetic and environmental sources of variation. However, we show that phenotypic plasticity is also present in that the proportion of eggs that enter diapause is influenced by environmental factors (temperature and light level) that vary seasonally. In nature there is typically a large parameter zone where environmental cues are somewhat correlated with seasonality, but not perfectly so, such that it may be advantageous to have a combination of both bet-hedging and plasticity. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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