The turquoise killifish, Nothobranchius furzeri, is a promising vertebrate model in ageing research and an emerging model organism in genomics, regenerative medicine, developmental biology and ecotoxicology. Its lifestyle is adapted to the ephemeral nature of shallow pools on the African savannah. Its rapid and short active life commences when rains fill the pool: fish hatch, grow rapidly and mature in as few as two weeks, and then reproduce daily until the pool dries out. Its embryos then become inactive, encased in the dry sediment and protected from the harsh environment until the rains return. This invertebrate-like life cycle (short active phase and long developmental arrest) combined with a vertebrate body plan provide the ideal attributes for a laboratory animal.

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

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Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J. Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evolutionary Biology. 2013;13:196. doi: 10.1186/1471-2148-13-196. PubMed DOI PMC

Bartáková V, Reichard M, Blažek R, Polačik M, Bryja J. Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. Journal of Biogeography. 2015;42:1832–1844. doi: 10.1111/jbi.12567. DOI

Baumgart M, Groth M, Priebe S, Savino A, Testa G, Dix A, Ripa R, Spallotta F, Gaetano C, Ori M, Terzibasi Tozzini E, Guthke R, Platzer M, Cellerino A. RNA-seq of the aging brain in the short-lived fish N. furzeri - conserved pathways and novel genes associated with neurogenesis. Aging Cell. 2014;13:965–974. doi: 10.1111/acel.12257. PubMed DOI PMC

Baumgart M, Barth E, Savino A, Groth M, Koch P, Petzold A, Arisi I, Platzer M, Marz M, Cellerino A. A miRNA catalogue and ncRNA annotation of the short-living fish Nothobranchius furzeri. BMC Genomics. 2017;18:693. doi: 10.1186/s12864-017-3951-8. PubMed DOI PMC

Blažek R, Polačik M, Reichard M. Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo. 2013;4:24. doi: 10.1186/2041-9139-4-24. PubMed DOI PMC

Blažek R, Polačik M, Kačer P, Cellerino A, Řežucha R, Methling C, Tomášek O, Syslová K, Terzibasi Tozzini E, Albrecht T, Vrtílek M, Reichard M. Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient. Evolution. 2017;71:386–402. doi: 10.1111/evo.13127. PubMed DOI

Cellerino A, Valenzano DR, Reichard M. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biological Reviews. 2016;91:511–533. doi: 10.1111/brv.12183. PubMed DOI

Dodzian J, Kean S, Seidel J, Valenzano DR. A protocol for laboratory housing of turquoise killifish (Nothobranchius furzeri) Journal of Visualized Experiments. 2018;134:57073. doi: 10.3791/57073. PubMed DOI PMC

Domínguez-Castanedo O, MÁ M-C, Valdesalici S. First observations of annualism in (Cyprinodontiformes: Rivulidae) Ichthyological Exploration of Freshwaters. 2013;24:15–20.

Domínguez-Castanedo O, Uribe MC, Rosales-Torres AM. Life history strategies of annual killifish Millerichthys robustus (Cyprinodontiformes:Cynolebiidae) in a seasonally ephemeral water body in Veracruz, México. Environmental Biology of Fishes. 2017;100:995–1006. doi: 10.1007/s10641-017-0617-y. DOI

Dorn A, Ng'oma E, Janko K, Reichwald K, Polačik M, Platzer M, Cellerino A, Reichard M. Phylogeny, genetic variability and colour polymorphism of an emerging animal model: the short-lived annual Nothobranchius fishes from southern Mozambique. Molecular Phylogenetics and Evolution. 2011;61:739–749. doi: 10.1016/j.ympev.2011.06.010. PubMed DOI

Frézal L, Félix M-A. C. elegans outside the Petri dish. eLife. 2015;4:e05849. doi: 10.7554/eLife.05849. PubMed DOI PMC

Furness AI, Lee K, Reznick DN. Adaptation in a variable environment: Phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish. Evolution. 2015a;69:1461–1475. doi: 10.1111/evo.12669. PubMed DOI

Furness AI, Reznick DN, Springer MS, Meredith RW. Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish. Proceedings of the Royal Society B: Biological Sciences. 2015b;282:20142189. doi: 10.1098/rspb.2014.2189. PubMed DOI PMC

Furness AI. The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause. Biological Reviews. 2016;91:796–812. doi: 10.1111/brv.12194. PubMed DOI

Graf M, Cellerino A, Englert C. Gender separation increases somatic growth in females but does not affect lifespan in Nothobranchius furzeri. PLoS One. 2010;5:e11958. doi: 10.1371/journal.pone.0011958. PubMed DOI PMC

Grégoir AF, Thoré ESJ, Philippe C, Pinceel T, Brendonck L, Vanschoenwinkel B. Squeezing out the last egg-annual fish increase reproductive efforts in response to a predation threat. Ecology and Evolution. 2018;8:6390–6398. doi: 10.1002/ece3.3422. PubMed DOI PMC

Haas R. Sexual selection in Nothobranchius guentheri (Pisces: Cyprinodontidae) Evolution. 1976a;30:614–622. doi: 10.1111/j.1558-5646.1976.tb00938.x. PubMed DOI

Haas R. Behavioral Biology of the Annual Killifish, Nothobranchius guentheri. Copeia. 1976b;1976:80–91. doi: 10.2307/1443776. DOI

Harel I, Benayoun BA, Machado B, Singh PP, Hu CK, Pech MF, Valenzano DR, Zhang E, Sharp SC, Artandi SE, Brunet A. A platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate. Cell. 2015;160:1013–1026. doi: 10.1016/j.cell.2015.01.038. PubMed DOI PMC

Harel I, Valenzano DR, Brunet A. Efficient genome engineering approaches for the short-lived African turquoise killifish. Nature Protocols. 2016;11:2010–2028. doi: 10.1038/nprot.2016.103. PubMed DOI

Hu CK, Brunet A. The African turquoise killifish: A research organism to study vertebrate aging and diapause. Aging cell. 2018;17:e12757. doi: 10.1111/acel.12757. PubMed DOI PMC

Jubb RA. A new Nothobranchius (Pisces, Cyprinodontidae) from Southeastern Rhodesia. Journal of American Killifish Association. 1971;8:12–19.

Matias JR, Markofsky J. The survival of embryos of the annual fish Nothobranchius guentheri exposed to temperature extremes and the subsequent effects on embryonic diapause. Journal of Experimental Zoology. 1978;204:219–227. doi: 10.1002/jez.1402040209. DOI

Neumann W. Eierlegende Zahnkarpfen. Marktheidenfeld, Germany: Schleunungdruck GmbH; 2008. Prachtgrunkärpflinge; p. 128.

Nezhybová V, Reichard M, Blažek R, Ondračková M. Metazoan parasites of African annual killifish (Nothobranchiidae): abundance, diversity, and their environmental correlates. Biotropica. 2017;49:229–238. doi: 10.1111/btp.12396. DOI

Ng'oma E, Groth M, Ripa R, Platzer M, Cellerino A. Transcriptome profiling of natural dichromatism in the annual fishes Nothobranchius furzeri and Nothobranchius kadleci. BMC Genomics. 2014;15:754. doi: 10.1186/1471-2164-15-754. PubMed DOI PMC

Parichy DM. Advancing biology through a deeper understanding of zebrafish ecology and evolution. eLife. 2015;4:e05635. doi: 10.7554/eLife.05635. PubMed DOI PMC

Passos C, Tassino B, Rosenthal GG, Reichard M. Reproductive behavior and sexual selection in annual fishes. In: Berois N, García G, de Sá R, editors. Annual Fishes: Life History Strategy, Diversity, and Evolution. CRC Press; 2015. pp. 207–229.

Petzold A, Reichwald K, Groth M, Taudien S, Hartmann N, Priebe S, Shagin D, Englert C, Platzer M. The transcript catalogue of the short-lived fish Nothobranchius furzeri provides insights into age-dependent changes of mRNA levels. BMC Genomics. 2013;14:185. doi: 10.1186/1471-2164-14-185. PubMed DOI PMC

Philippe C, Hautekiet P, Grégoir AF, Thoré ESJ, Pinceel T, Stoks R, Brendonck L, Boeck G. Combined effects of cadmium exposure and temperature on the annual killifish (Nothobranchius furzeri) Environmental Toxicology and Chemistry. 2018;37:2361–2371. doi: 10.1002/etc.4182. PubMed DOI

Podrabsky JE, Carpenter JF, Hand SC. Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2001;280:R123–R131. doi: 10.1152/ajpregu.2001.280.1.R123. PubMed DOI

Podrabsky JE, Garrett ID, Kohl ZF. Alternative developmental pathways associated with diapause regulated by temperature and maternal influences in embryos of the annual killifish Austrofundulus limnaeus. Journal of Experimental Biology. 2010;213:3280–3288. doi: 10.1242/jeb.045906. PubMed DOI PMC

Podrabsky JE, Hand SC. The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. Journal of Experimental biology. 1999;202:2567–2580. PubMed

Podrabsky JE, Riggs CL, Romney AL, Woll SC, Wagner JT, Culpepper KM, Cleaver TG. Embryonic development of the annual killifish Austrofundulus limnaeus: An emerging model for ecological and evolutionary developmental biology research and instruction. Developmental Dynamics. 2017;246:779–801. doi: 10.1002/dvdy.24513. PubMed DOI

Polačik M, Reichard M. Indirect fitness benefits are not related to male dominance in a killifish. Behavioral Ecology and Sociobiology. 2009;63:1427–1435. doi: 10.1007/s00265-009-0798-2. DOI

Polačik M, Reichard M. Diet overlap among three sympatric African annual killifish species Nothobranchius spp. from Mozambique. Journal of Fish Biology. 2010;77:754–768. doi: 10.1111/j.1095-8649.2010.02717.x. PubMed DOI

Polačik M, Donner MT, Reichard M. Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? Journal of Fish Biology. 2011;78:796–809. doi: 10.1111/j.1095-8649.2010.02893.x. PubMed DOI

Polačik M, Reichard M. Asymmetric reproductive isolation between two sympatric annual killifish with extremely short lifespans. PLoS One. 2011;6:e22684. doi: 10.1371/journal.pone.0022684. PubMed DOI PMC

Polačik M, Harrod C, Blažek R, Reichard M. Trophic niche partitioning in communities of African annual fish: evidence from stable isotopes. Hydrobiologia. 2014a;721:99–106. doi: 10.1007/s10750-013-1652-0. DOI

Polačik M, Blažek R, Režucha R, Vrtílek M, Terzibasi Tozzini E, Reichard M. Alternative intrapopulation life-history strategies and their trade-offs in an African annual fish. Journal of Evolutionary Biology. 2014b;27:854–865. doi: 10.1111/jeb.12359. PubMed DOI

Polačik M, Blažek R, Reichard M. Laboratory breeding of the short-lived annual killifish Nothobranchius furzeri. Nature Protocols. 2016;11:1396–1413. doi: 10.1038/nprot.2016.080. PubMed DOI

Polačik M, Smith C, Reichard M. Maternal source of variability in the embryo development of an annual killifish. Journal of Evolutionary Biology. 2017;30:738–749. doi: 10.1111/jeb.13038. PubMed DOI

Polačik M, Reichard M, Vrtílek M. Local variation in embryo development rate in annual fish. Journal of Fish Biology. 2018;92:1359–1370. doi: 10.1111/jfb.13591. PubMed DOI

Reichard M, Polacik M, Sedlácek O. Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span. Journal of Fish Biology. 2009;74:198–212. doi: 10.1111/j.1095-8649.2008.02129.x. PubMed DOI

Reichard M, Polačik M, Blažek R, Vrtílek M. Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evolutionary Ecology. 2014;28:1105–1120. doi: 10.1007/s10682-014-9732-9. DOI

Reichard M, Cellerino A, Valenzano DR. Turquoise killifish. Current Biology. 2015;25:R741–R742. doi: 10.1016/j.cub.2015.05.009. PubMed DOI

Reichard M. The evolutionary ecology of African annual fishes. In: Berois N, García G, de Sá R, editors. Annual Fishes: Life History Strategy, Diversity, and Evolution. CRC Press; 2015. pp. 133–158.

Reichard M, Janáč M, Polačik M, Blažek R, Vrtílek M. Community assembly in Nothobranchius annual fishes: Nested patterns, environmental niche and biogeographic history. Ecology and Evolution. 2017a;7:2294–2306. doi: 10.1002/ece3.2851. PubMed DOI PMC

Reichard M, Blažek R, Polačik M, Vrtílek M. Hatching date variability in wild populations of four coexisting species of African annual fishes. Developmental Dynamics. 2017b;246:827–837. doi: 10.1002/dvdy.24500. PubMed DOI

Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N, Pietsch S, Baumgart M, Chalopin D, Felder M, Bens M, Sahm A, Szafranski K, Taudien S, Groth M, Arisi I, Weise A, Bhatt SS, Sharma V, Kraus JM, Schmid F, Priebe S, Liehr T, Görlach M, Than ME, Hiller M, Kestler HA, Volff JN, Schartl M, Cellerino A, Englert C, Platzer M. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell. 2015;163:1527–1538. doi: 10.1016/j.cell.2015.10.071. PubMed DOI

Sedláček O, Baciaková B, Kratochvíl L. Evolution of body colouration in killifishes (Cyprinodontiformes: Aplocheilidae, Nothobranchiidae, Rivulidae): Is male ornamentation constrained by intersexual genetic correlation? Zoologischer Anzeiger - A Journal of Comparative Zoology. 2014;253:207–215. doi: 10.1016/j.jcz.2013.12.004. DOI

Smith P, Willemsen D, Popkes M, Metge F, Gandiwa E, Reichard M, Valenzano DR. Regulation of life span by the gut microbiota in the short-lived African turquoise killifish. eLife. 2017;6:e27014. doi: 10.7554/eLife.27014. PubMed DOI PMC

Terzibasi E, Valenzano DR, Benedetti M, Roncaglia P, Cattaneo A, Domenici L, Cellerino A. Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One. 2008;3:e3866. doi: 10.1371/journal.pone.0003866. PubMed DOI PMC

Thoré ESJ, Steenaerts L, Philippe C, Grégoir A, Brendonck L, Pinceel T. Individual behavioral variation reflects personality divergence in the upcoming model organism Nothobranchius furzeri. Ecology and Evolution. 2018;8:8448–8457. doi: 10.1002/ece3.4356. PubMed DOI PMC

Tozzini ET, Dorn A, Ng'oma E, Polačik M, Blažek R, Reichwald K, Petzold A, Watters B, Reichard M, Cellerino A. Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evolutionary Biology. 2013;13:77. doi: 10.1186/1471-2148-13-77. PubMed DOI PMC

Valdesalici S, Cellerino A. Extremely short lifespan in the annual fish Nothobranchius furzeri. Proceedings of the Royal Society B: Biological Sciences. 2003;270 Suppl 2:S189–S191. doi: 10.1098/rsbl.2003.0048. PubMed DOI PMC

Valenzano DR, Kirschner J, Kamber RA, Zhang E, Weber D, Cellerino A, Englert C, Platzer M, Reichwald K, Brunet A. Mapping loci associated with tail color and sex determination in the short-lived fish Nothobranchius furzeri. Genetics. 2009;183:1385–1395. doi: 10.1534/genetics.109.108670. PubMed DOI PMC

Valenzano DR, Benayoun BA, Singh PP, Zhang E, Etter PD, Hu CK, Clément-Ziza M, Willemsen D, Cui R, Harel I, Machado BE, Yee MC, Sharp SC, Bustamante CD, Beyer A, Johnson EA, Brunet A. The african turquoise killifish genome provides insights into evolution and genetic architecture of lifespan. Cell. 2015;163:1539–1554. doi: 10.1016/j.cell.2015.11.008. PubMed DOI PMC

Vrtílek M, Reichard M. Highly plastic resource allocation to growth and reproduction in females of an African annual fish. Ecology of Freshwater Fish. 2015;24:616–628. doi: 10.1111/eff.12175. DOI

Vrtílek M, Reichard M. Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient. Ecology and Evolution. 2016;6:5921–5931. doi: 10.1002/ece3.2337. PubMed DOI PMC

Vrtílek M, Žák J, Pšenička M, Reichard M. Extremely rapid maturation of a wild African annual fish. Current Biology. 2018a;28:R822–R824. doi: 10.1016/j.cub.2018.06.031. PubMed DOI

Vrtílek M, Žák J, Blažek R, Polačik M, Cellerino A, Reichard M. Limited scope for reproductive senescence in wild populations of a short-lived fish. The Science of Nature. 2018b;105:68. doi: 10.1007/s00114-018-1594-5. PubMed DOI

Vrtílek M, Žák J, Polačik M, Blažek R, Reichard M. Longitudinal demographic study of wild populations of African annual killifish. Scientific Reports. 2018c;8:4774. doi: 10.1038/s41598-018-22878-6. PubMed DOI PMC

Watters BR. The ecology and distribution of Nothobranchius fishes. The Journal of the American Killifish Association. 2009;42:37–76.

Wendler S, Hartmann N, Hoppe B, Englert C. Age-dependent decline in fin regenerative capacity in the short-lived fish Nothobranchius furzeri. Aging Cell. 2015;14:857–866. doi: 10.1111/acel.12367. PubMed DOI PMC

Woll SC, Podrabsky JE. Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus. The Journal of Experimental Biology. 2017;220:2777–2786. doi: 10.1242/jeb.151373. PubMed DOI

Wourms JP. The developmental biology of annual fishes. 3. Pre-embryonic and embryonic diapause of variable duration in the eggs of annual fishes. Journal of Experimental Zoology. 1972;182:389–414. doi: 10.1002/jez.1401820310. PubMed DOI

Žák J, Reichard M, Gvoždík L. Limited differentiation of fundamental thermal niches within the killifish assemblage from shallow temporary waters. Journal of Thermal Biology. 2018;78:257–262. doi: 10.1016/j.jtherbio.2018.10.015. PubMed DOI

RNAseq Analysis of Brain Aging in Wild Specimens of Short-Lived Turquoise Killifish: Commonalities and Differences With Aging Under Laboratory Conditions

Patterns and drivers of Nothobranchius killifish diversity in lowland Tanzania

Good performance of turquoise killifish (Nothobranchius furzeri) on pelleted diet as a step towards husbandry standardization

Genetic diversity of a widespread annual killifish from coastal Tanzania