Embryo-environment interactions are of paramount importance during the development of all organisms, and impacts during this period can echo far into later stages of ontogeny. African annual fish of the genus Nothobranchius live in temporary pools and their eggs survive the dry season in the dry bottom substrate of the pools by entering a facultative developmental arrest termed diapause. Uniquely among animals, the embryos (encased in eggs) may enter diapause at three different developmental stages. Such a system allows for the potential to employ different regulation mechanisms for each diapause. We sampled multiple Nothobranchius embryo banks across the progressing season, species, and populations. We present important baseline field data and examine the role of environmental regulation in the embryonic development of this unique system. We describe the course of embryo development in the wild and find it to be very different from the typical development under laboratory conditions. Development across the embryo banks was synchronized within and across the sampled populations with all embryos entering diapause I during the rainy season and diapause II during the dry season. Asynchrony occurred at transient phases of the habitat, during the process of habitat desiccation, and at the end of the dry season. Our findings reveal the significance of environmental conditions in the serial character of the annual fish diapauses.

Center for Life in Extreme Environments Portland State University Portland OR USA

Department of Zoology Charles University Prague Czech Republic

Institute of Vertebrate Biology The Czech Academy of Sciences Brno Czech Republic

Zobrazit více v PubMed

Bartáková, V. , Nagy, B. , Polačik, M. , Blažek, R. , Lamtane, H. , & Reichard, M. (2020). Genetic diversity of a widespread annual killifish from coastal Tanzania. BMC Evolutionary Biology, 20, 1. 10.1186/s12862-019-1549-2 PubMed DOI PMC

Bates, D. , Maechler, M. , Bolker, B. , & Walker, S. (2015). Fitting linear mixed‐effects models using {lme4}. Journal of Statistical Software, 67(1), 1–48.

Berois, N. , García, G. , & de Sá, R. O. (2015). Annual Fishes: Life history strategy, diversity, and evolution. CRC Press.

Cáceres, C. E. (1997). Dormancy in invertebrates. Invertebrate Biology, 116, 371–383. 10.2307/3226870 DOI

Cellerino, A. , Valenzano, D. R. , & 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. PubMed

Childs, D. Z. , Metcalf, C. J. E. , & Rees, M. (2010). Evolutionary bet‐hedging in the real world: Empirical evidence and challenges revealed by plants. Proceedings of the Royal Society B: Biological Sciences, 277(1697), 3055–3064. PubMed PMC

Dodzian, J. , Kean, S. , Seidel, J. , & Valenzano, D. R. (2018). A protocol for laboratory housing of turquoise killifish (Nothobranchius furzeri). Journal of Visualized Experiments, 134, e57073. PubMed PMC

Dolfi, L. , Ripa, R. , Antebi, A. , Valenzano, D. R. , & Cellerino, A. (2019). Cell cycle dynamics during diapause entry and exit in an annual killifish revealed by FUCCI technology. EvoDevo, 10(1), 1–22. 10.1186/s13227-019-0142-5 PubMed DOI PMC

Domínguez‐Castanedo, O. , Uribe, M. C. , & Rosales‐Torres, A. M. (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(8), 995–1006. 10.1007/s10641-017-0617-y DOI

Eckerström‐Liedholm, S. , Sowersby, W. , Gonzalez‐Voyer, A. , & Rogell, B. (2017). Time‐limited environments affect the evolution of egg‐body size allometry. Evolution, 71, 1900–1910. 10.1111/evo.13286 PubMed DOI

Furness, A. I. , Lee, K. , & Reznick, D. N. (2015). Adaptation in a variable environment: Phenotypic plasticity and bet‐hedging during egg diapause and hatching in an annual killifish. Evolution, 69, 1461–1475. 10.1111/evo.12669 PubMed DOI

Furness, A. I. , Reznick, D. N. , Springer, M. S. , & Meredith, R. W. (2015). Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish. Proceedings of the Royal Society B: Biological Sciences, 282(1802), 2014–2189. PubMed PMC

García, D. , Loureiro, M. , & Tassino, B. (2008). Reproductive behavior in the annual fish Austrolebias reicherti Loureiro & García 2004 (Cyprinodontiformes: Rivulidae). Neotropical Ichthyology, 6, 243–248.

Hand, S. C. (1991). Metabolic dormancy in aquatic invertebrates. In Castellini M. A. (Ed.), Advances in comparative and environmental physiology. Springer.

Hand, S. C. , Denlinger, D. L. , Podrabsky, J. E. , & Roy, R. (2016). Mechanisms of animal diapause: Recent developments from nematodes, crustaceans, insects, and fish. American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology, 310, R1193–R1211. 10.1152/ajpregu.00250.2015 PubMed DOI PMC

Helmstetter, A. J. , Papadopulos, A. S. , Igea, J. , Van Dooren, T. J. , Leroi, A. M. , & Savolainen, V. (2016). Viviparity stimulates diversification in an order of fish. Nature Communications, 7(1), 1–7. 10.1038/ncomms11271 PubMed DOI PMC

Hu, C. K. , & Brunet, A. (2018). The African turquoise killifish: A research organism to study vertebrate aging and diapause. Aging Cell, 17, e12757. 10.1111/acel.12757 PubMed DOI PMC

Hu, C.‐K. , Wang, W. , Brind’Amour, J. , Singh, P. P. , Reeves, G. A. , Lorincz, M. C. , Alvarado, A. S. , & Brunet, A. (2020). Vertebrate diapause preserves organisms long term through Polycomb complex members. Science, 367, 870–874. 10.1126/science.aaw2601 PubMed DOI PMC

Inglima, K. , Perlmutter, A. , & Markovsky, J. (1981). Reversible stage‐specific embryonic inhibition mediated by the presence of adults in the annual fish Nothobranchius guentheri . Journal of Experimental Zoology, 215, 23–33. 10.1002/jez.1402150104 PubMed DOI

Košťál, V. (2006). Eco‐physiological phases of insect diapause. Journal of Insect Physiology, 52, 113–127. 10.1016/j.jinsphys.2005.09.008 PubMed DOI

Levels, P. J. , & Denucé, J. M. (1988). Intrinsic variability in the frequency of embryonic diapauses of the annual fish Nothobranchius korthausae, regulated by light: Dark cycle and temperature. Environmental Biology of Fishes, 22(3), 211–224. 10.1007/BF00005382 DOI

Levels, P. J. , Gubbels, R. E. , & Denucé, J. M. (1986). Oxygen consumption during embryonic development of the annual fish Nothobranchius korthausae with special reference to diapause. Comparative Biochemistry and Physiology A, Comparative Physiology, 84, 767–770. 10.1016/0300-9629(86)90403-2 PubMed DOI

Markofsky, J. , & Matias, J. R. (1977). The effects of temperature and season of collection on the onset and duration of diapause in embryos of the annual fish Nothobranchius guentheri . Journal of Experimental Zoology, 202, 49–56. 10.1002/jez.1402020107 PubMed DOI

Matias, J. R. , & 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. 10.1002/jez.1402040209 DOI

Nagy, B. , & Kis, A. H. (2010). Variation in habitat characteristics and the occurrence of Nothobranchius species in seasonal biotopes of Tanzania. Journal of the American Kilifish Association, 43, 130–144.

Papa, N. G. , Clivio, G. A. , & Montagne, J. (2015). Husbandry, reproduction, and embryo culture of annual fishes under laboratory conditions. In Berois N., García G., & de Sá R. O. (Eds.), Annual Fishes: Life history strategy, diversity, and evolution (pp. 99–107). CRC Press.

Peters, N. (1963). Embryonale Anpassungen oviparer Zahnkarpfen aus periodisch austrocknenden Gewässern. Internationale Revue Der Gesamten Hydrobiologie Und Hydrographie, 48, 257–313. 10.1002/iroh.19630480204 DOI

Pinceel, T. , Vanschoenwinkel, B. , Deckers, P. , Grégoir, A. , Ver Eecke, T. , & Brendonck, L. (2015). Early and late developmental arrest as complementary embryonic bet‐hedging strategies in African killifish. Biological Journal of the Linnean Society, 114, 941–948. 10.1111/bij.12474 DOI

Podrabsky, J. E. , Carpenter, J. F. , & Hand, S. C. (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. 10.1152/ajpregu.2001.280.1.R123 PubMed DOI

Podrabsky, J. E. , Garrett, I. D. F. , & Kohl, Z. F. (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. 10.1242/jeb.045906 PubMed DOI PMC

Podrabsky, J. E. , & Hand, S. C. (1999). The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus . Journal of Experimental Biology, 202, 2567–2580. PubMed

Podrabsky, J. E. , & Hand, S. C. (2015). Physiological strategies during animal diapause: Lessons from brine shrimp and annual killifish. Journal of Experimental Biology, 218(12), 1897–1906. 10.1242/jeb.116194 PubMed DOI PMC

Podrabsky, J. E. , Lopez, J. P. , Fan, T. W. M. , Higashi, R. , & Somero, G. N. (2007). Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: Insights from a metabolomics analysis. Journal of Experimental Biology, 210, 2253–2266. 10.1242/jeb.005116 PubMed DOI

Podrabsky, J. E. , Riggs, C. L. , Romney, A. L. , Woll, S. C. , Wagner, J. T. , Culpepper, K. M. , & Cleaver, T. G. (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. PubMed

Podrabsky, J. , Riggs, C. , & Wagner, J. (2016). Tolerance of environmental stress. In Berois N., García G. & de Sá R.O. (Eds.), Annual fishes. Life history strategy, diversity, and evolution (pp. 159–184).CRC Press.

Podrabsky, J. E. , Romney, A. L. , & Culpepper, K. M. (2015). Alternative developmental pathways. In Berois N., Graciela G., & Rafael O. D. S. (Eds.), Annual fishes: Life history strategy, diversity, and evolution. CRC Press.

Polačik, M. , Blažek, R. , & Reichard, M. (2016). Laboratory breeding of the short‐lived annual killifish Nothobranchius furzeri . Nature Protocols, 11, 1396–1413. 10.1038/nprot.2016.080 PubMed DOI

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

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

R Core Team . (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.r‐project.org/

Reichard, M. (2015). The evolutionary ecology of African annual fishes. In Berois N., García G., & de Sá R. O. (Eds.), Annual Fishes: Life history strategy, diversity, and evolution. CRC Press.

Reichard, M. , Polačik, M. , & Sedláček, O. (2009). Distribution, colour polymorphism and habitat use of the African killifish, Nothobranchius furzeri, the vertebrate with the shortest lifespan. Journal of Fish Biology, 74, 198–212. PubMed

Romney, A. L. T. , Davis, E. M. , Corona, M. M. , Wagner, J. T. , & Podrabsky, J. E. (2018). Temperature‐dependent vitamin D signaling regulates developmental trajectory associated with diapause in an annual killifish. Proceedings of the National Academy of Sciences, 115, 12763–12768. 10.1073/pnas.1804590115 PubMed DOI PMC

Romney, A. L. T. , & Podrabsky, J. E. (2017). Epigenetic regulation of alternative developmental trajectories. The FASEB Journal, 31, 595.2.

Shidlovsky, K. (2010). Collecting Nothobranchius in south‐western Tanzania. Nothobranchius Archives, 1, 18–27.

Simons, A. M. (2011). Modes of response to environmental change and the elusive empirical evidence for bet‐hedging. Proceedings of the Royal Society B, 278, 1601–1609. 10.1098/rspb.2011.0176 PubMed DOI PMC

Slater, P. , & Milinski, M. (1996). Parental Care: Evolution, Mechanisms, and Adaptive Significance. Academic Press.

Strachan, S. R. , Chester, E. T. , & Robson, B. J. (2015). Freshwater invertebrate life history strategies for surviving desiccation. Springer Science Reviews, 3, 57–75. 10.1007/s40362-015-0031-9 DOI

Volcan, M. V. , Gonçalves, A. C. , Lanés, L. E. K. , & Guadagnin, D. L. (2015). Annual fishes (Rivulidae) from Southern Brazil: A Broad‐Scale assessment of their diversity and conservation. In Berois N., García G., & de Sá R. O. (Eds.), Annual Fishes: Life history strategy, diversity, and evolution. CRC Press.

Vrtílek, M. , & 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. 10.1002/ece3.2337 PubMed DOI PMC

Vrtílek, M. , Žák, J. , Polačik, M. , Blažek, R. , & Reichard, M. (2018). Longitudinal demographic study of wild populations of African annual killifish. Scientific Reports, 8, 4774. PubMed PMC

Watters, B. R. (2009). The ecology and distribution of Nothobranchius fishes. Journal of the American Killifish Association, 42, 37–76.

Watters, B. R. , Nagy, B. , van der Merwe, P. D. , Cotterill, F. P. , & Bellstedt, D. U. (2020). Redescription of the seasonal killifish species Nothobranchius ocellatus and description of a related new species Nothobranchius matanduensis, from eastern Tanzania.

Westerink, R. M. (1996). Evaluation of monthly precipitation data of Mozambique. Nota Técnica, 69, 1–156.

Wilson, J. G. (1973). Environment and birth defects. Academic Press.

Wourms, J. P. (1972a). The developmental biology of annual fishes I. Stages in the normal development of Austrofundulus myersi Dahl. Journal of Experimental Zoology, 182, 143–168. PubMed

Wourms, J. P. (1972b). The developmental biology of annual fishes II. Naturally occurring dispersion and reaggregation of blastomeres during the development of annual fish eggs. Journal of Experimental Zoology, 182, 169–200. PubMed

Wourms, J. P. (1972c). The developmental biology of annual fishes III. Pre‐embryonic and embryonic diapause of variable duration in the eggs of annual fishes. Journal of Experimental Zoology, 182, 389–414. PubMed

Patterns and drivers of Nothobranchius killifish diversity in lowland Tanzania

Zobrazit více v PubMed

Dryad
10.5061/dryad.cc2fqz65k