The African savannah is dotted with ephemeral freshwater pools known as water pans, which form during the rainy season. Killifishes of the genus Nothobranchius, colloquially called annual fishes, have adapted to live in these pools. Popular with specialist aquarium hobbyists for their stunning colouration, most of 75 described species are available in captivity (Neumann, 2008), which is how Nothobranchius furzeri first made its way into research laboratories worldwide. Alessandro Cellerino, a physiologist from Scuola Normale Superiore in Pisa, Italy, was intrigued by an incredibly short-lived population of the annual fish that his friend Stefano Valdesalici bred at home. Experimental investigation of its lifespan revealed that the fish matured after just four weeks, after which their mortality increased sharply from the age of six weeks and all the fish died within 10 weeks (Valdesalici and Cellerino, 2003). The fish of this strain were named GRZ after Gona Re Zhou National Park in Zimbabwe where the fish were originally collected in 1970 (Jubb, 1971). They were later found to live slightly longer as housing conditions developed (Cellerino et al., 2016), though it remains the shortest-lived population of N. furzeri yet recorded. Collection trips to Mozambique and Zimbabwe between 2004 and 2016 assembled a set of populations that vary in lifespan and possess a variable level of inbreeding (Terzibasi et al., 2008; Cellerino et al., 2016; Reichard et al., 2017a).

The remarkably short lifespan of N. furzeri recapitulates the hallmarks of vertebrate ageing (Harel et al., 2015), condensed into few weeks and responsive to pharmacological, dietary and lifestyle interventions (Cellerino et al., 2016). Its genome has been sequenced and assembled (Valenzano et al., 2015; Reichwald et al., 2015), and there are transcriptomes for a number of its tissues (Petzold et al., 2013; Baumgart et al., 2014; Baumgart et al., 2017). Several inbred lines are also available (Hu and Brunet, 2018) and genome-editing techniques are widely adopted to rapidly produce stable transgenic lines too (Harel et al., 2016). With this background, N. furzeri has reached outside the world of ageing research and has become valuable for studies in such disparate branches of investigation as evolutionary genomics (Reichwald et al., 2015), regenerative medicine (Wendler et al., 2015), developmental biology (Hu and Brunet, 2018) and ecotoxicology (Philippe et al., 2018). Here, we explore how our understanding of the natural history of the species makes a key contribution to the development of this species as a laboratory model.

The life cycle of N. furzeri is adapted to the transient nature of its habitat and is strictly separated into two distinct phases. The first phase starts when fish hatch after their pool is inundated with rainwater and immediately start feeding. Explosive juvenile growth brings them to sexual maturity in as little as two weeks, growing from the initial size of 5 mm to 30–50 mm over that period (Vrtílek et al., 2018a). Growth slows thereafter as resources are diverted to reproduction, but a body size of 75 mm can be reached in males after 10–15 weeks (Blažek et al., 2013; Vrtílek et al., 2018a). Importantly, their growth rate is strongly dependent on population density and food availability; fish in dense populations are typically small and sexually immature at an age of 3–5 weeks, both in the wild and in the laboratory (Graf et al., 2010; Grégoir et al., 2018; Philippe et al., 2018; Vrtílek et al., 2018a). Individual fish vary in growth rates (Blažek et al., 2013), perhaps reflecting variation in personality traits (Thoré et al., 2018). Upon sexual maturity, females lay eggs daily. A typical fecundity of 20–120 eggs per day was estimated in wild populations, with more variation among populations than among females within a sample (Vrtílek and Reichard, 2016; Vrtílek et al., 2018b), seemingly in response to resource availability.

All adult fish die when their pool desiccates, but mortality is strong over the entire lifespan (Vrtílek et al., 2018c). In longer-lasting pools (persisting more than four months), fish often disappear despite the habitat still appearing capable of supporting them. The fish likely succumb to a combination of predation by birds, bouts of extremely high water temperatures, decreased water quality from organic input by visiting animals, low dissolved oxygen levels, exhaustion of resources, and physiological deterioration as a trade-off to rapid juvenile development (Reichard, 2015). While wild-derived, outbred N. furzeri populations have a maximum lifespan (defined as 90% survival at the population level) of 25–42 weeks in captivity (Terzibasi et al., 2008; Tozzini et al., 2013; Blažek et al., 2017), only one of 13 N. furzeri populations monitored in the wild survived beyond the age of 17 weeks and most disappeared at the age of 3–10 weeks as their habitat dried up (Vrtílek et al., 2018c). After desiccation, dry sediment retains the eggs in a dormant state (diapause); an adaptation to the harsh environmental conditions, over the entire dry season that lasts 5–11 months (Cellerino et al., 2016; Vrtílek et al., 2018b).

N. furzeri is distributed in southern Mozambique, with a few populations extending to adjacent parts of southern Zimbabwe, only few kilometres across the border (Figure 1A). Interestingly, the range of N. furzeri lies on a gradient in aridity associated with distance from the coast. Evaporation, the amount of rainfall and its predictability are major environmental factors that vary across that gradient (Terzibasi et al., 2008; Tozzini et al., 2013; Polačik et al., 2018), with the driest and least predictable conditions furthest from the ocean (and at the highest altitude) (Figure 1A). N. furzeri is absent in the wettest region, where another two Nothobranchius species, that otherwise coexist with N. furzeri, maintain viable populations. In contrast, N. furzeri is the most common Nothobranchius species in the dry region, 90–400 km from the coast and 19–220 m above sea level (Reichard et al., 2017a). Two isolated Zimbabwean populations are found even higher, at 325–340 m above sea level. To date, we have located and georeferenced 90 N. furzeri populations over its entire range and their geographic coordinates are accessible at the Figshare repository (doi: 10.6084/m9.figshare.7017167). Our sampling was limited by accessibility from roads and there are many more N. furzeri populations scattered throughout the Mozambican mopane and miombo woodlands and Acacia savannah.

Figure 1

Download asset Open asset

Local pools vary greatly in size and shrink gradually (Vrtílek et al., 2018b) (Figure 2A–B). Environmental conditions in the pool may be harsh; water temperature can fluctuate between 20 and 36°C from early morning to late afternoon (Reichard et al., 2009; Žák et al., 2018). Late in the season (in May), morning water temperature can drop to 15°C. Fine sediment is repeatedly disturbed by cattle (which have functionally replaced the wild African megafauna) (Figure 2C) and partially dissolves in water, producing extremely turbid conditions (Figure 2D). However, in cases when the pool is thickly overgrown with vegetation (Figure 2E) and undisturbed by domestic cattle, the water can be transparent.

Figure 2

Download asset Open asset

Two distinct colour morphs of male N. furzeri occur, often coexisting in the same population (Reichard et al., 2009). The "yellow" morph (Figure 1B) possesses a yellow crescent marking along the outer margin of the caudal fin, outlined by a black margin. "Red" morph males (Figure 1C) have red caudal fins. The extent of colouration on the caudal fin varies widely among wild populations, but the two morphs are clearly discrete (Valenzano et al., 2009; Ng'oma et al., 2014). The black margin of the caudal fin is also present in some populations of red males and exceptionally absent in yellow males. Female colouration is dull and brownish and shows no indication of polymorphism (Figure 1D).

The geographic distribution of the morphs suggests a link between male colouration and adaptations to different habitat conditions. The yellow morph dominates dry, marginal parts of the range, with exclusively yellow males in the driest region of Zimbabwe. Red males dominate populations in the wet part of the range (Figure 1A) (Reichard et al., 2009; Dorn et al., 2011). This contrast is mirrored in the colouration of the most common laboratory strains, with the short-lived GRZ comprising exclusively yellow males while the longer-lived MZM0403 are exclusively red (Cellerino et al., 2016). Interestingly, most natural populations are polymorphic (Figure 1A) and no differences in life history traits between red and yellow males have been established where they coexist. While it is tempting to associate male colouration with adaptation to dry and wet conditions, there is no evidence of any causal link so far.

Populations of N. furzeri are divided into two main phylogeographic clades (named Chefu and Limpopo), with limited secondary contact (Terzibasi et al., 2008; Bartáková et al., 2013; Figure 1A). The populations are strongly structured, with rare dispersal between them. The population genetic signature reveals that the Chefu clade has recently experienced dramatic population expansion (Dorn et al., 2011) and demonstrated linkage between populations along the small rivulet basins (Bartáková et al., 2015). Hence, large floods, occurring in exceptionally wet years, are assumed to provide the main mode of dispersal between populations (Reichard, 2015). Surprisingly for a fish, large rivers form boundaries in the distribution of clades and species, including a division of the Limpopo clade to two subclades (Figure 1G) and a boundary between the range of N. furzeri and its sister species, N. kadleci (Bartáková et al., 2015).

N. furzeri are opportunistic and generalist predators of small invertebrates. In general, the diet reflects prey availability in particular pools. Small crustaceans (Cladocera, Copepoda, and Ostracoda) typically constitute more than 70% of digested prey, with insect larvae also being a common prey item (Polačik and Reichard, 2010). Backswimmers (nothonectid bugs) are common in the pools but underrepresented in the diet. Chironomid larvae, the most common diet of N. furzeri in the laboratory, are also consumed by wild N. furzeri (Polačik and Reichard, 2010). The diet of N. furzeri differs from the two coexisting species (N. orthonotus and N. pienaari) when prey is abundant though all species resort to any available food of a suitable size when choice is limited (Polačik et al., 2014a). The diet is reflected in the intestinal microbiome and wild N. furzeri populations differ in the microbial composition of their guts (Smith et al., 2017). Interestingly, laboratory fish possess the core microbiota of wild N. furzeri and reconstitution of high microbial diversity in old fish extends their lifespan in the laboratory (Smith et al., 2017).

All Nothobranchius species are sexually dimorphic (Sedláček et al., 2014). Male colouration and mating behaviour appear strongly sexually selected (Haas, 1976a). Males compete aggressively for access to females and large males are dominant (Polačik and Reichard, 2009). Females express mate choice by approaching a displaying male. Males actively pursue females and may coerce spawning (Polačik and Reichard, 2011). The elaborate male colouration is puzzling, as N. furzeri often live in extremely turbid water where visibility is minimal. Indeed, male colouration fades in turbid water. Courtship is brief; the male approaches a female and stops to perform lateral displays with his unpaired fins extended. A receptive female allows the male to fold her in his dorsal fin and the female lays an egg into the sediment. During oviposition, the pair jerks and the sediment is disturbed. With the aid of stiffened rays of the anal fin, the egg is deposited slightly into the substrate (Passos et al., 2015). Most eggs are found at pool margins (M. Polačik, unpublished data). There is no consistent choice of red or yellow males by individual N. furzeri females (Reichard and Polačik, unpublished data) and mate choice appears to be based on other traits.

Reproduction occurs primarily in the morning. The eggs are ovulated just after sunrise (07:00-08:00) (Haas, 1976b) and by 10:00 some females have already spawned all their ovulated eggs. Most females are spent by 15:00 and a new batch of eggs is ovulated next morning (Vrtílek and Reichard, 2016). Daily fecundity is strongly contingent upon long-term (the effect of body mass: Vrtílek and Reichard, 2016) and short-term (the effect of ration on the preceding day: Vrtílek and Reichard, 2015) access to resources.

The embryonic phase of the N. furzeri life cycle represents the longest but least understood part of the life cycle in the wild. All Nothobranchius populations are limited to pools with a special type of substrate composed of an alkaline swelling clay (Watters, 2009), the physical and chemical properties of which are crucial for the survival of N. furzeri eggs. Annual killifish possess three dormancy stages occurring at defined developmental points (Wourms, 1972) (Box 1). Watters, 2009 proposed a model of natural embryo development of Nothobranchius that links embryo developmental with three phases of incubation conditions (wet, dry and humid) (Box 1).

Large variability in embryo developmental dynamics is a key feature for the long-term persistence of N. furzeri populations in their highly unpredictable environment (Furness, 2016), serving as an effective bet-hedging strategy against false hatching cues, such as insufficient rainfall (Polačik et al., 2017). Erratic rains and mid-season desiccation generate conditions for two (or perhaps even more) generations or cohorts in some years (Reichard et al., 2017b).

Laboratory research in N. furzeri and other annual killifishes has suggested that developmental disparity is achieved through maternal effects, perhaps based on RNA or protein products. Interestingly, embryos of young females tend to develop rapidly while embryos of older females tend to halt development at diapause (Podrabsky et al., 2010; Polačik et al., 2017); a seeming adaptation to the possibility of a second inundation in a single rainy season that the eggs of young females experience more often than the eggs of older females (Polačik et al., 2014b). However, in the wild the beginning and end of diapause, at least in other killifish species, appears to be controlled by environmental factors (Matias and Markofsky, 1978; Podrabsky et al., 2010; Domínguez-Castanedo et al., 2017) and developmental variability may be achieved through habitat heterogeneity rather than intrinsic control. Gradual desiccation and vertical distribution of embryos create a cline of incubation conditions that generate a staggered embryo development.

The course of embryo development has marked impacts on post-hatching lifespan. Rapidly developing embryos produce phenotypes with a rapid post-hatching strategy, typified by a smaller size at hatching but more rapid growth and sexual maturation, and smaller final size and shorter lifespan (Polačik et al., 2014b). It remains to be identified whether embryonic diapause is causally responsible for the limited rapid development later in life, representing one of the outstanding questions to be addressed (Box 2). Intriguingly, in a Neotropical annual killifish, insulin-like growth factor signalling regulates developmental trajectories (Woll and Podrabsky, 2017), representing candidate regulatory pathway for killifish life history.

The key advantage of N. furzeri as a model species stems from the combination of its rapid post-hatching lifestyle and long phase of embryonic arrest that can be altered by manipulating environmental conditions. Having a model with a vertebrate body plan and invertebrate-like life history and lifespan (i.e. short and rapid active lifespan and dormant stage) is a valuable characteristic beyond the field of ageing research, not least because researchers are often constrained by the duration of grant funding. The arrested stage makes the species ideal for storing and shipping and permits flexible time management when working with this 'instant' fish (Polačik et al., 2016). In addition, given harsh and variable conditions in natural habitats, captive N. furzeri does not require any precise conditions for water quality and housing, perhaps except access to abundant and nutrient rich food (Polačik et al., 2016; Dodzian et al., 2018).

Information on wild N. furzeri populations, and particularly the environmental gradient in its range, have been especially instrumental in explaining differences in lifespan among captive strains (Tozzini et al., 2013; Blažek et al., 2017) and in validating that its rapid life history is not an artefact of the laboratory (Vrtílek et al., 2018a; Vrtílek et al., 2018c). Field studies have also strengthened conclusions on the role of microbiota on ageing (Smith et al., 2017) and genomic insights into the evolution of short lifespan (Valenzano et al., 2015; Reichwald et al., 2015). Formulating a standardised artificial diet that would be readily consumed by captive N. furzeri now appears critical to increase experimental repeatability across laboratories. Detailed understanding of the natural diet of N. furzeri (Polačik and Reichard, 2010; Polačik et al., 2014a) should help the community to accomplish this goal.

Compared to other fish model systems in biomedical research (e.g. Parichy, 2015), our understanding of the natural history of N. furzeri is substantial (Cellerino et al., 2016). Indeed, N. furzeri may, uniquely, be a model that bridges the interests of ecological and biomedical research (Cellerino et al., 2016). Still, we know relatively little about some features of the natural history of N. furzeri. While some pressing issues are outlined in Box 2, we highlight that the greatest gap in our knowledge of the natural life cycle of N. furzeri is in understanding embryonic development under natural conditions. Data from wild populations demonstrated that high phenotypic plasticity of N. furzeri, manifested in the laboratory by individually disparate growth rates, timing of sexual maturation and fecundity, is natural. While perhaps complicating some experimental designs, it raises a multitude of questions on the underlying mechanisms, from gene expression to individual behaviour (Box 2). With much more to be discovered on the natural history of the species, we anticipate that N. furzeri will continue to be instrumental in showing how conceptual and methodological insights from ecological and biomedical research can be integrated within a single research agenda (Reichard et al., 2015; Cellerino et al., 2016).

1. 1. Bartáková V
   2. Reichard M
   3. Janko K
   4. Polačik M
   5. Blažek R
   6. Reichwald K
   7. Cellerino A
   8. Bryja J

   (2013) Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique

   BMC Evolutionary Biology 13:196.

   https://doi.org/10.1186/1471-2148-13-196

   • PubMed
   • Google Scholar
2. 1. Bartáková V
   2. Reichard M
   3. Blažek R
   4. Polačik M
   5. Bryja J

   (2015) Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna

   Journal of Biogeography 42:1832–1844.

   https://doi.org/10.1111/jbi.12567

   • Google Scholar
3. 1. Baumgart M
   2. Groth M
   3. Priebe S
   4. Savino A
   5. Testa G
   6. Dix A
   7. Ripa R
   8. Spallotta F
   9. Gaetano C
   10. Ori M
   11. Terzibasi Tozzini E
   12. Guthke R
   13. Platzer M
   14. Cellerino A

   (2014) RNA-seq of the aging brain in the short-lived fish N. furzeri - conserved pathways and novel genes associated with neurogenesis

   Aging Cell 13:965–974.

   https://doi.org/10.1111/acel.12257

   • PubMed
   • Google Scholar
4. 1. Baumgart M
   2. Barth E
   3. Savino A
   4. Groth M
   5. Koch P
   6. Petzold A
   7. Arisi I
   8. Platzer M
   9. Marz M
   10. Cellerino A

   (2017) A miRNA catalogue and ncRNA annotation of the short-living fish Nothobranchius furzeri

   BMC Genomics 18:693.

   https://doi.org/10.1186/s12864-017-3951-8

   • PubMed
   • Google Scholar
5. 1. Blažek R
   2. Polačik M
   3. Reichard M

   (2013) Rapid growth, early maturation and short generation time in African annual fishes

   EvoDevo 4:24.

   https://doi.org/10.1186/2041-9139-4-24

   • PubMed
   • Google Scholar
6. 1. Blažek R
   2. Polačik M
   3. Kačer P
   4. Cellerino A
   5. Řežucha R
   6. Methling C
   7. Tomášek O
   8. Syslová K
   9. Terzibasi Tozzini E
   10. Albrecht T
   11. Vrtílek M
   12. Reichard M

   (2017) Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient

   Evolution 71:386–402.

   https://doi.org/10.1111/evo.13127

   • PubMed
   • Google Scholar
7. 1. Cellerino A
   2. Valenzano DR
   3. Reichard M

   (2016) From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology

   Biological Reviews 91:511–533.

   https://doi.org/10.1111/brv.12183

   • PubMed
   • Google Scholar
8. 1. Dodzian J
   2. Kean S
   3. Seidel J
   4. Valenzano DR

   (2018) A protocol for laboratory housing of turquoise killifish (Nothobranchius furzeri)

   Journal of Visualized Experiments 134:57073.

   https://doi.org/10.3791/57073

   • Google Scholar
9. 1. Domínguez-Castanedo O
   2. MÁ M-C
   3. Valdesalici S

   (2013)

   First observations of annualism in (Cyprinodontiformes: Rivulidae)

   Ichthyological Exploration of Freshwaters 24:15–20.

   • Google Scholar
10. 1. Domínguez-Castanedo O
    2. Uribe MC
    3. Rosales-Torres AM

    (2017) Life history strategies of annual killifish Millerichthys robustus (Cyprinodontiformes:Cynolebiidae) in a seasonally ephemeral water body in Veracruz, México

    Environmental Biology of Fishes 100:995–1006.

    https://doi.org/10.1007/s10641-017-0617-y

    • Google Scholar
11. 1. Dorn A
    2. Ng'oma E
    3. Janko K
    4. Reichwald K
    5. Polačik M
    6. Platzer M
    7. Cellerino A
    8. Reichard M

    (2011) Phylogeny, genetic variability and colour polymorphism of an emerging animal model: the short-lived annual Nothobranchius fishes from southern Mozambique

    Molecular Phylogenetics and Evolution 61:739–749.

    https://doi.org/10.1016/j.ympev.2011.06.010

    • PubMed
    • Google Scholar
12. 1. Frézal L
    2. Félix M-A

    (2015) C. elegans outside the Petri dish

    eLife 4:e05849.

    https://doi.org/10.7554/eLife.05849

    • Google Scholar
13. 1. Furness AI
    2. Lee K
    3. Reznick DN

    (2015a) Adaptation in a variable environment: Phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish

    Evolution 69:1461–1475.

    https://doi.org/10.1111/evo.12669

    • Google Scholar
14. 1. Furness AI
    2. Reznick DN
    3. Springer MS
    4. Meredith RW

    (2015b) Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish

    Proceedings of the Royal Society B: Biological Sciences 282:20142189.

    https://doi.org/10.1098/rspb.2014.2189

    • Google Scholar
15. 1. Furness AI

    (2016) The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause

    Biological Reviews 91:796–812.

    https://doi.org/10.1111/brv.12194

    • PubMed
    • Google Scholar
16. 1. Graf M
    2. Cellerino A
    3. Englert C

    (2010) Gender separation increases somatic growth in females but does not affect lifespan in Nothobranchius furzeri

    PLoS One 5:e11958.

    https://doi.org/10.1371/journal.pone.0011958

    • PubMed
    • Google Scholar
17. 1. Grégoir AF
    2. Thoré ESJ
    3. Philippe C
    4. Pinceel T
    5. Brendonck L
    6. Vanschoenwinkel B

    (2018) Squeezing out the last egg-annual fish increase reproductive efforts in response to a predation threat

    Ecology and Evolution 8:6390–6398.

    https://doi.org/10.1002/ece3.3422

    • PubMed
    • Google Scholar
18. 1. Haas R

    (1976a) Sexual selection in Nothobranchius guentheri (Pisces: Cyprinodontidae)

    Evolution 30:614–622.

    https://doi.org/10.1111/j.1558-5646.1976.tb00938.x

    • Google Scholar
19. 1. Haas R

    (1976b) Behavioral Biology of the Annual Killifish, Nothobranchius guentheri

    Copeia 1976:80–91.

    https://doi.org/10.2307/1443776

    • Google Scholar
20. 1. Harel I
    2. Benayoun BA
    3. Machado B
    4. Singh PP
    5. Hu CK
    6. Pech MF
    7. Valenzano DR
    8. Zhang E
    9. Sharp SC
    10. Artandi SE
    11. Brunet A

    (2015) A platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate

    Cell 160:1013–1026.

    https://doi.org/10.1016/j.cell.2015.01.038

    • PubMed
    • Google Scholar
21. 1. Harel I
    2. Valenzano DR
    3. Brunet A

    (2016) Efficient genome engineering approaches for the short-lived African turquoise killifish

    Nature Protocols 11:2010–2028.

    https://doi.org/10.1038/nprot.2016.103

    • PubMed
    • Google Scholar
22. 1. Hu CK
    2. Brunet A

    (2018) The African turquoise killifish: A research organism to study vertebrate aging and diapause

    Aging cell 17:e12757.

    https://doi.org/10.1111/acel.12757

    • PubMed
    • Google Scholar
23. 1. Jubb RA

    (1971)

    A new Nothobranchius (Pisces, Cyprinodontidae) from Southeastern Rhodesia

    Journal of American Killifish Association 8:12–19.

    • Google Scholar
24. 1. Matias JR
    2. Markofsky J

    (1978) 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 204:219–227.

    https://doi.org/10.1002/jez.1402040209

    • Google Scholar
25. 1. Neumann W

    (2008)

    Eierlegende Zahnkarpfen

    128, Prachtgrunkärpflinge, Eierlegende Zahnkarpfen, Marktheidenfeld, Germany, Schleunungdruck GmbH.

    • Google Scholar
26. 1. Nezhybová V
    2. Reichard M
    3. Blažek R
    4. Ondračková M

    (2017) Metazoan parasites of African annual killifish (Nothobranchiidae): abundance, diversity, and their environmental correlates

    Biotropica 49:229–238.

    https://doi.org/10.1111/btp.12396

    • Google Scholar
27. 1. Ng'oma E
    2. Groth M
    3. Ripa R
    4. Platzer M
    5. Cellerino A

    (2014) Transcriptome profiling of natural dichromatism in the annual fishes Nothobranchius furzeri and Nothobranchius kadleci

    BMC Genomics 15:754.

    https://doi.org/10.1186/1471-2164-15-754

    • PubMed
    • Google Scholar
28. 1. Parichy DM

    (2015) Advancing biology through a deeper understanding of zebrafish ecology and evolution

    eLife 4:e05635.

    https://doi.org/10.7554/eLife.05635

    • Google Scholar
29. Book

    1. Passos C
    2. Tassino B
    3. Rosenthal GG
    4. Reichard M

    (2015)

    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. pp. 207–229.

    • Google Scholar
30. 1. Petzold A
    2. Reichwald K
    3. Groth M
    4. Taudien S
    5. Hartmann N
    6. Priebe S
    7. Shagin D
    8. Englert C
    9. Platzer M

    (2013) The transcript catalogue of the short-lived fish Nothobranchius furzeri provides insights into age-dependent changes of mRNA levels

    BMC Genomics 14:185.

    https://doi.org/10.1186/1471-2164-14-185

    • PubMed
    • Google Scholar
31. 1. Philippe C
    2. Hautekiet P
    3. Grégoir AF
    4. Thoré ESJ
    5. Pinceel T
    6. Stoks R
    7. Brendonck L
    8. Boeck G

    (2018) Combined effects of cadmium exposure and temperature on the annual killifish (Nothobranchius furzeri)

    Environmental Toxicology and Chemistry 37:2361–2371.

    https://doi.org/10.1002/etc.4182

    • PubMed
    • Google Scholar
32. 1. Podrabsky JE
    2. Carpenter JF
    3. Hand SC

    (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers

    American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 280:R123–R131.

    https://doi.org/10.1152/ajpregu.2001.280.1.R123

    • PubMed
    • Google Scholar
33. 1. Podrabsky JE
    2. Garrett ID
    3. Kohl ZF

    (2010) Alternative developmental pathways associated with diapause regulated by temperature and maternal influences in embryos of the annual killifish Austrofundulus limnaeus

    Journal of Experimental Biology 213:3280–3288.

    https://doi.org/10.1242/jeb.045906

    • PubMed
    • Google Scholar
34. 1. Podrabsky JE
    2. Hand SC

    (1999)

    The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus

    Journal of Experimental biology 202:2567–2580.

    • PubMed
    • Google Scholar
35. 1. Podrabsky JE
    2. Riggs CL
    3. Romney AL
    4. Woll SC
    5. Wagner JT
    6. Culpepper KM
    7. Cleaver TG

    (2017) Embryonic development of the annual killifish Austrofundulus limnaeus: An emerging model for ecological and evolutionary developmental biology research and instruction

    Developmental Dynamics 246:779–801.

    https://doi.org/10.1002/dvdy.24513

    • PubMed
    • Google Scholar
36. 1. Polačik M
    2. Reichard M

    (2009) Indirect fitness benefits are not related to male dominance in a killifish

    Behavioral Ecology and Sociobiology 63:1427–1435.

    https://doi.org/10.1007/s00265-009-0798-2

    • Google Scholar
37. 1. Polačik M
    2. Reichard M

    (2010) Diet overlap among three sympatric African annual killifish species Nothobranchius spp. from Mozambique

    Journal of Fish Biology 77:754–768.

    https://doi.org/10.1111/j.1095-8649.2010.02717.x

    • PubMed
    • Google Scholar
38. 1. Polačik M
    2. Donner MT
    3. Reichard M

    (2011) Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony?

    Journal of Fish Biology 78:796–809.

    https://doi.org/10.1111/j.1095-8649.2010.02893.x

    • PubMed
    • Google Scholar
39. 1. Polačik M
    2. Reichard M

    (2011) Asymmetric reproductive isolation between two sympatric annual killifish with extremely short lifespans

    PLoS One 6:e22684.

    https://doi.org/10.1371/journal.pone.0022684

    • PubMed
    • Google Scholar
40. 1. Polačik M
    2. Harrod C
    3. Blažek R
    4. Reichard M

    (2014a) Trophic niche partitioning in communities of African annual fish: evidence from stable isotopes

    Hydrobiologia 721:99–106.

    https://doi.org/10.1007/s10750-013-1652-0

    • Google Scholar
41. 1. Polačik M
    2. Blažek R
    3. Režucha R
    4. Vrtílek M
    5. Terzibasi Tozzini E
    6. Reichard M

    (2014b) Alternative intrapopulation life-history strategies and their trade-offs in an African annual fish

    Journal of Evolutionary Biology 27:854–865.

    https://doi.org/10.1111/jeb.12359

    • PubMed
    • Google Scholar
42. 1. Polačik M
    2. Blažek R
    3. Reichard M

    (2016) Laboratory breeding of the short-lived annual killifish Nothobranchius furzeri

    Nature Protocols 11:1396–1413.

    https://doi.org/10.1038/nprot.2016.080

    • PubMed
    • Google Scholar
43. 1. Polačik M
    2. Smith C
    3. Reichard M

    (2017) Maternal source of variability in the embryo development of an annual killifish

    Journal of Evolutionary Biology 30:738–749.

    https://doi.org/10.1111/jeb.13038

    • PubMed
    • Google Scholar
44. 1. Polačik M
    2. Reichard M
    3. Vrtílek M

    (2018) Local variation in embryo development rate in annual fish

    Journal of Fish Biology 92:1359–1370.

    https://doi.org/10.1111/jfb.13591

    • PubMed
    • Google Scholar
45. 1. Reichard M
    2. Polacik M
    3. Sedlácek O

    (2009) Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span

    Journal of Fish Biology 74:198–212.

    https://doi.org/10.1111/j.1095-8649.2008.02129.x

    • PubMed
    • Google Scholar
46. 1. Reichard M
    2. Polačik M
    3. Blažek R
    4. Vrtílek M

    (2014) Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors

    Evolutionary Ecology 28:1105–1120.

    https://doi.org/10.1007/s10682-014-9732-9

    • Google Scholar
47. 1. Reichard M
    2. Cellerino A
    3. Valenzano DR

    (2015) Turquoise killifish

    Current Biology 25:R741–R742.

    https://doi.org/10.1016/j.cub.2015.05.009

    • Google Scholar
48. Book

    1. Reichard M

    (2015)

    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. pp. 133–158.

    • Google Scholar
49. 1. Reichard M
    2. Janáč M
    3. Polačik M
    4. Blažek R
    5. Vrtílek M

    (2017a) Community assembly in Nothobranchius annual fishes: Nested patterns, environmental niche and biogeographic history

    Ecology and Evolution 7:2294–2306.

    https://doi.org/10.1002/ece3.2851

    • PubMed
    • Google Scholar
50. 1. Reichard M
    2. Blažek R
    3. Polačik M
    4. Vrtílek M

    (2017b) Hatching date variability in wild populations of four coexisting species of African annual fishes

    Developmental Dynamics 246:827–837.

    https://doi.org/10.1002/dvdy.24500

    • PubMed
    • Google Scholar
51. 1. Reichwald K
    2. Petzold A
    3. Koch P
    4. Downie BR
    5. Hartmann N
    6. Pietsch S
    7. Baumgart M
    8. Chalopin D
    9. Felder M
    10. Bens M
    11. Sahm A
    12. Szafranski K
    13. Taudien S
    14. Groth M
    15. Arisi I
    16. Weise A
    17. Bhatt SS
    18. Sharma V
    19. Kraus JM
    20. Schmid F
    21. Priebe S
    22. Liehr T
    23. Görlach M
    24. Than ME
    25. Hiller M
    26. Kestler HA
    27. Volff JN
    28. Schartl M
    29. Cellerino A
    30. Englert C
    31. Platzer M

    (2015) Insights into sex chromosome evolution and aging from the genome of a short-lived fish

    Cell 163:1527–1538.

    https://doi.org/10.1016/j.cell.2015.10.071

    • PubMed
    • Google Scholar
52. 1. Sedláček O
    2. Baciaková B
    3. Kratochvíl L

    (2014) 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 253:207–215.

    https://doi.org/10.1016/j.jcz.2013.12.004

    • Google Scholar
53. 1. Smith P
    2. Willemsen D
    3. Popkes M
    4. Metge F
    5. Gandiwa E
    6. Reichard M
    7. Valenzano DR

    (2017) Regulation of life span by the gut microbiota in the short-lived African turquoise killifish

    eLife 6:e27014.

    https://doi.org/10.7554/eLife.27014

    • PubMed
    • Google Scholar
54. 1. Terzibasi E
    2. Valenzano DR
    3. Benedetti M
    4. Roncaglia P
    5. Cattaneo A
    6. Domenici L
    7. Cellerino A

    (2008) Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri

    PLoS One 3:e3866.

    https://doi.org/10.1371/journal.pone.0003866

    • PubMed
    • Google Scholar
55. 1. Thoré ESJ
    2. Steenaerts L
    3. Philippe C
    4. Grégoir A
    5. Brendonck L
    6. Pinceel T

    (2018) Individual behavioral variation reflects personality divergence in the upcoming model organism Nothobranchius furzeri

    Ecology and Evolution 8:8448–8457.

    https://doi.org/10.1002/ece3.4356

    • PubMed
    • Google Scholar
56. 1. Tozzini ET
    2. Dorn A
    3. Ng'oma E
    4. Polačik M
    5. Blažek R
    6. Reichwald K
    7. Petzold A
    8. Watters B
    9. Reichard M
    10. Cellerino A

    (2013) Parallel evolution of senescence in annual fishes in response to extrinsic mortality

    BMC Evolutionary Biology 13:77.

    https://doi.org/10.1186/1471-2148-13-77

    • PubMed
    • Google Scholar
57. 1. Valdesalici S
    2. Cellerino A

    (2003) Extremely short lifespan in the annual fish Nothobranchius furzeri

    Proceedings of the Royal Society B: Biological Sciences 270 Suppl 2:S189–S191.

    https://doi.org/10.1098/rsbl.2003.0048

    • PubMed
    • Google Scholar
58. 1. Valenzano DR
    2. Kirschner J
    3. Kamber RA
    4. Zhang E
    5. Weber D
    6. Cellerino A
    7. Englert C
    8. Platzer M
    9. Reichwald K
    10. Brunet A

    (2009) Mapping loci associated with tail color and sex determination in the short-lived fish Nothobranchius furzeri

    Genetics 183:1385–1395.

    https://doi.org/10.1534/genetics.109.108670

    • PubMed
    • Google Scholar
59. 1. Valenzano DR
    2. Benayoun BA
    3. Singh PP
    4. Zhang E
    5. Etter PD
    6. Hu CK
    7. Clément-Ziza M
    8. Willemsen D
    9. Cui R
    10. Harel I
    11. Machado BE
    12. Yee MC
    13. Sharp SC
    14. Bustamante CD
    15. Beyer A
    16. Johnson EA
    17. Brunet A

    (2015) The african turquoise killifish genome provides insights into evolution and genetic architecture of lifespan

    Cell 163:1539–1554.

    https://doi.org/10.1016/j.cell.2015.11.008

    • PubMed
    • Google Scholar
60. 1. Vrtílek M
    2. Reichard M

    (2015) Highly plastic resource allocation to growth and reproduction in females of an African annual fish

    Ecology of Freshwater Fish 24:616–628.

    https://doi.org/10.1111/eff.12175

    • Google Scholar
61. 1. Vrtílek M
    2. Reichard M

    (2016) Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient

    Ecology and Evolution 6:5921–5931.

    https://doi.org/10.1002/ece3.2337

    • PubMed
    • Google Scholar
62. 1. Vrtílek M
    2. Žák J
    3. Pšenička M
    4. Reichard M

    (2018a) Extremely rapid maturation of a wild African annual fish

    Current Biology 28:R822–R824.

    https://doi.org/10.1016/j.cub.2018.06.031

    • PubMed
    • Google Scholar
63. 1. Vrtílek M
    2. Žák J
    3. Blažek R
    4. Polačik M
    5. Cellerino A
    6. Reichard M

    (2018b) Limited scope for reproductive senescence in wild populations of a short-lived fish

    The Science of Nature 105:68.

    https://doi.org/10.1007/s00114-018-1594-5

    • Google Scholar
64. 1. Vrtílek M
    2. Žák J
    3. Polačik M
    4. Blažek R
    5. Reichard M

    (2018c) Longitudinal demographic study of wild populations of African annual killifish

    Scientific Reports 8:4774.

    https://doi.org/10.1038/s41598-018-22878-6

    • PubMed
    • Google Scholar
65. 1. Watters BR

    (2009)

    The ecology and distribution of Nothobranchius fishes

    The Journal of the American Killifish Association 42:37–76.

    • Google Scholar
66. 1. Wendler S
    2. Hartmann N
    3. Hoppe B
    4. Englert C

    (2015) Age-dependent decline in fin regenerative capacity in the short-lived fish Nothobranchius furzeri

    Aging Cell 14:857–866.

    https://doi.org/10.1111/acel.12367

    • PubMed
    • Google Scholar
67. 1. Woll SC
    2. Podrabsky JE

    (2017) Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

    The Journal of Experimental Biology 220:2777–2786.

    https://doi.org/10.1242/jeb.151373

    • PubMed
    • Google Scholar
68. 1. Wourms JP

    (1972) 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 182:389–414.

    https://doi.org/10.1002/jez.1401820310

    • PubMed
    • Google Scholar
69. 1. Žák J
    2. Reichard M
    3. Gvoždík L

    (2018) Limited differentiation of fundamental thermal niches within the killifish assemblage from shallow temporary waters

    Journal of Thermal Biology 78:257–262.

    https://doi.org/10.1016/j.jtherbio.2018.10.015

    • PubMed
    • Google Scholar

Thank you for submitting your article "The Natural History of Model Organisms: Nothobranchius furzeri, an 'instant' fish from an ephemeral habitat" for consideration by eLife. Your article has been reviewed by three peer reviewers, and the evaluation has been overseen by two Features Editors at eLife (Stuart King and Peter Rodgers). The following individuals involved in review of your submission have agreed to reveal their identity: Andrew Furness and Dario Riccardo Valenzano.

After a consultation with the reviewers, the editor has drafted this decision to help you prepare a revised submission.

Summary:

This essay is being considered as part of a series of articles on "The Natural History of Model Organisms" (https://elifesciences.org/collections/8de90445/the-natural-history-of-model-organisms). Each article should explain how our knowledge of the natural history of a model organism has informed recent advances in biology, and how understanding its natural history can influence/advance future studies.

This article summarizes what is known of the natural history of the turquoise killifish (Nothobranchius furzeri), an interesting model organism that is gaining traction in several fields of investigation. The manuscript is compelling, clear and easy to read. However, a number of details should be attended to prior to publication.

The editor may also contact you separately about some editorial or stylistic issues that will need to be addressed.

Essential revisions:

1) The sections in the article provide a comprehensive introduction to the natural history of N. furzeri. However, more should be done to address "how our understanding of the natural history of the species makes a key contribution to its development as a laboratory model" (as stated in the Introduction). Please revise the sections to emphasise how knowledge of N. furzeri's natural history has benefited researchers working with this species in the lab, and/or discoveries in specific fields mentioned in the Introduction. This change would help the article to stand out from other recent (and less-recent) general reviews on N. furzeri as a model system in biology (e.g. Terzibasi et al., 2008; Reichard et al., 2015; Cellerino et al., 2016; Hu et al., 2018).

2) Despite the raising interest about N. furzeri by the scientific community, the reviewers felt it was an overstatement to refer to it as "an established vertebrate model in ageing research" and "the species of choice in […] evolutionary genomics, regenerative medicine, developmental biology and ecotoxicology". This text should be toned down. The revised text should aim to give a more balanced view (i.e. pros and cons) of how the natural history of the species contributes to its usefulness as a model organism. (Brief comparisons with other model organisms, including invertebrates and other vertebrates, could be considered to add wider context or strengthen arguments.)

3) Some of the cited work on killifish diapause and reproduction is from species besides N. furzeri; yet the way the references are cited does not make this clear to a reader unfamiliar with the system. Please include a 'disclaimer' somewhere in the text to indicate that what is known about diapause/development is drawn from studies of other related annual killifish, and although many aspects seem to be highly congruent among species, it remains to be determined whether the same applies to N. furzeri specifically.

4) The main text mentions that little is known about the development in the wild. As such, please consider including at least one or two question about the developmental pathways of N. furzeri embryos in the wild into the "Outstanding questions" in Box 2.

5) The paper currently includes 60 references, 28 of which are directly from the two authors. Though the authors have majorly contributed to the development of N. furzeri as a biomedical and ecological system, they should consider if all these citations are needed and if other articles have been missed from the reference list.

Essential revisions:

1) The sections in the article provide a comprehensive introduction to the natural history of N. furzeri. However, more should be done to address "how our understanding of the natural history of the species makes a key contribution to its development as a laboratory model" (as stated in the Introduction). Please revise the sections to emphasise how knowledge of N. furzeri's natural history has benefited researchers working with this species in the lab, and/or discoveries in specific fields mentioned in the Introduction. This change would help the article to stand out from other recent (and less-recent) general reviews on N. furzeri as a model system in biology (e.g. Terzibasi et al., 2008; Reichard et al., 2015; Cellerino et al., 2016; Hu et al., 2018).

We entirely agree with that comment. Ironically, we deleted a special paragraph in the “Key advantages” section in the first version of the manuscript during the final pruning of the text. This section is now included (subsection “Key advantages of N. furzeri for the model species role”) and it recapitulates the most instrumental insights that knowledge of natural history of the species benefits lab research. We also included what we see is the current major limitation of N. furzeri as a model animal – the lack of artificial standardised diet that would be consumed by adult fish where data from natural populations are crucial. We initially believed that this is outside of the scope of the “natural history” but we now see that lack of this important aspect would be misleading.

In addition, we expanded the section on gut microbiota where that link is very strong (subsection “Diet”) and highlighted the lack of knowledge on immune responses despite the turquoise killifish are faced with multitude of infections in nature and are capable to respond to them immunologically (subsection “Parasites”).

2) Despite the raising interest about N. furzeri by the scientific community, the reviewers felt it was an overstatement to refer to it as "an established vertebrate model in ageing research" and "the species of choice in […] evolutionary genomics, regenerative medicine, developmental biology and ecotoxicology". This text should be toned down. The revised text should aim to give a more balanced view (i.e. pros and cons) of how the natural history of the species contributes to its usefulness as a model organism. (Brief comparisons with other model organisms, including invertebrates and other vertebrates, could be considered to add wider context or strengthen arguments.)

We toned down those statements and refer to N. furzeri as "promising model in ageing" (Abstract) or "emerging model" (in some other disciplines).

"…become the species of choice…" has been replaced by "…become available for studies…"

We also pay more attention to compare the pros and cons of N. furzeri with other model animals, specifically highlighting "invertebrate-like" life history that is beneficial for laboratory breeding and vertebrate body plan (and this rationale is better explained in the current version of the manuscript).

3) Some of the cited work on killifish diapause and reproduction is from species besides N. furzeri; yet the way the references are cited does not make this clear to a reader unfamiliar with the system. Please include a 'disclaimer' somewhere in the text to indicate that what is known about diapause/development is drawn from studies of other related annual killifish, and although many aspects seem to be highly congruent among species, it remains to be determined whether the same applies to N. furzeri specifically.

Such disclaimer is now included in the main text ("Laboratory research in N. furzeri and other annual killifishes has suggested…"; "…diapause, at least in other killifish species, appears to be…") and in Box 1 ("While this developmental pathway appears strikingly congruent across all annual killifish clades (Furness et al., 2015b), it remains to be determined whether it also fully applies to N. furzeri.")

4) The main text mentions that little is known about the development in the wild. As such, please consider including at least one or two question about the developmental pathways of N. furzeri embryos in the wild into the "Outstanding questions" in Box 2.

That question is now included: "How do N. furzeri embryos develop under natural conditions? Current knowledge of the embryo development comes from laboratory conditions. As incubation in the lab largely differs from natural conditions, we need to know how much its diverges from the natural course of development."

5) The paper currently includes 60 references, 28 of which are directly from the two authors. Though the authors have majorly contributed to the development of N. furzeri as a biomedical and ecological system, they should consider if all these citations are needed and if other articles have been missed from the reference list.

We are aware of this unfortunate bias. This is primarily driven by the fact that we are indeed the only research group working on the ecology and evolution of wild populations of N. furzeri and this review specifically aims at the natural history of the species. We have tried to minimize that bias by including more reference to laboratory studies that investigated aspects of natural history of the species. There are now six new references from other teams added: Grégoir et al., 2017; Thoré et al., 2018, Woll and Podrabsky 2017, Dodzian et al., 2018, and Domiguez-Castanedo et al., 2013; Furness et al., 2015b), although we also added two relevant studies from our team that are highly relevant to the review (on thermoregulation and reproductive senescence in the wild).

Author details

1. Martin Reichard

   Martin Reichard is at the Czech Academy of Sciences, Institute of Vertebrate Biology, Brno, Czech Republic

   For correspondence

   reichard@ivb.cz

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9306-0074

2. Matej Polačik

   Matej Polačik is at the Czech Academy of Sciences, Institute of Vertebrate Biology, Brno, Czech Republic

   Competing interests

   No competing interests declared

• 6,084

  views

• 544

  downloads

• 51

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.