Reproductive senescence is an age-associated decline in reproductive performance, which often arises as a trade-off between current and future reproduction. Given that mortality is inevitable, increased allocation into current reproduction is favoured despite costs paid later in life. This assumption is violated in organisms with post-maturity growth whose reproductive output increases long after maturity. While reproductive senescence is frequently studied in animals with determinate growth at maturity, such as insects or mammals, we have very limited understanding of reproductive senescence in organisms with an extensive post-maturity growth period. The fact that many post-maturity growers experience strong adult mortality leads to conflicting expectations for reproductive senescence. The aim of this study was to investigate how co-occurrence of rapid life history and post-maturity growth mould reproductive senescence in a short-lived killifish, Nothobranchius furzeri, using longitudinal data on laboratory and wild-type populations. We followed the individual fecundity, fertility and fertilization of 132 singly housed fish from the perspectives of chronological and biological age. At the onset of senescence, the sex-specific contribution to decrease in fertilization capacity was investigated. Allocation trade-offs were estimated through the association between reproductive parameters and life span, and between early-life and late-life fecundity. We demonstrate that female fecundity increased steadily after maturity and reproductive senescence occurred long after the growth asymptote. The prime age for fecundity coincided with 50% female survival and consequent decline in fecundity implies an association with somatic deterioration. Reproductive senescence in fertilization rate was stronger in females than in males. Females with high early fecundity experienced a long life span and high late-life fecundity, discounting the role of allocation trade-offs in reproductive senescence. The present study reports a clear case of reproductive senescence in a fish with a long post-maturation growth period, unusually rapid development and short life span. The onset of reproductive senescence was postponed compared to animals that cease growing at sexual maturity. Fish and other animals with post-maturity growth have long been considered insusceptible to ageing but this conclusion may be related to the previous lack of longitudinal data rather than to the absence of reproductive senescence in such organisms.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Zoology Faculty of Science Charles University Prague Czech Republic

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

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Arslan, R. C., Willführ, K. P., Frans, E. M., Verweij, K. J. H., Bürkner, P.-C., Myrskylä, M., Voland, E., Almqvist, C., Zietsch, B. P., & Penke, L. (2017). Older fathers’ children have lower evolutionary fitness across four centuries and in four populations. Proceedings of the Royal Society B: Biological Sciences, 284, 20171562. https://doi.org/10.1098/rspb.2017.1562

Austad, S. N., & Hoffman, J. M. (2018). Is antagonistic pleiotropy ubiquitous in aging biology? Evolution, Medicine and Public Health, 2018(1), 287-294. https://doi.org/10.1093/emph/eoy033

Barneche, D. R., Robertson, D. R., White, C. R., & Marshall, D. J. (2018). Fish reproductive-energy output increases disproportionately with body size. Science, 645(May), 642-645. https://doi.org/10.1126/science.aao6868

Bartáková, V., Reichard, M., Janko, K., Polačik, M., Blažek, R., Reichwald, K., Cellerino, A., & 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

Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using {lme4}. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01

Benoît, H. P., Swain, D. P., Hutchings, J. A., Knox, D., Doniol-Valcroze, T., & Bourne, C. M. (2018). Evidence for reproductive senescence in a broadly distributed harvested marine fish. Marine Ecology Progress Series, 592, 207-224. https://doi.org/10.3354/meps12532

Bidder, G. P. (1932). Senescence. The British Medical Journal, 2(3742), 583-585. https://doi.org/10.1136/bmj.2.3742.583

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. (2017). Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient. Evolution, 71(2), 386-402. https://doi.org/10.1111/evo.13127

Blažek, R., Polačik, M., & 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

Bonduriansky, R., Maklakov, A., Zajitschek, F., & Brooks, R. (2008). Sexual selection, sexual conflict and the evolution of ageing and life span. Functional Ecology, 22(3), 443-453. https://doi.org/10.1111/j.1365-2435.2008.01417.x

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(2), 511-533. https://doi.org/10.1111/brv.12183

Charnov, E. L., Turner, T. F., & Winemiller, K. O. (2001). Reproductive constraints and the evolution of life histories with indeterminate growth. Proceedings of the National Academy of Sciences of the United States of America, 98, 9460-9464. https://doi.org/10.1073/pnas.161294498

Cornwallis, C. K., Dean, R., & Pizzari, T. (2014). Sex-specific patterns of aging in sexual ornaments and gametes. The American Naturalist, 184(3), E66-E78. https://doi.org/10.1086/677385

Cui, R., Medeiros, T., Willemsen, D., Iasi, L. N. M., Collier, G. E., Graef, M., Reichard, M., & Valenzano, D. R. (2019). Relaxed selection limits lifespan by increasing mutation load. Cell, 178(2), 385-399. https://doi.org/10.1016/j.cell.2019.06.004

Depeux, C., Lemaître, J.-F., Moreau, J., Dechaume-Moncharmont, F.-X., Laverre, T., Pauhlac, H., Gaillard, J.-M., & Beltran-Bech, S. (2020). Reproductive senescence and parental effects in an indeterminate grower. Journal of Evolutionary Biology. https://doi.org/10.1111/jeb.13667

DeRose, M. A., & Roff, D. A. (1999). A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution, 53(4), 1288-1292. https://doi.org/10.1111/j.1558-5646.1999.tb04541.x

Di Cicco, E., Terzibasi Tozzini, E., Rossi, G., & Cellerino, A. (2011). The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Experimental Gerontology, 46(4), 249-256. https://doi.org/10.1016/j.exger.2010.10.011

Dolfi, L., Suen, T. K., Ripa, R., & Antebi, A. (2020). Optimization of cryopreservation and in vitro fertilization techniques for the African turquoise killifish Nothobranchius furzeri. BioarXiv. https://doi.org/10.1101/2020.04.14.040824

Eckhardt, F., Kappeler, P. M., & Kraus, C. (2017). Highly variable lifespan in an annual reptile, Labord's chameleon (Furcifer labordi). Scientific Reports, 7(1), 7-11. https://doi.org/10.1038/s41598-017-11701-3

Finch, C. E. (1990). Senescence and the genome. University of Chicago Press.

Finch, C. E. (1998). Variations in senescence and longevity include the possibility of negligible senescence. Journals of Gerontology - Series A: Biological Sciences, 53(4), 235-239. https://doi.org/10.1093/gerona/53A.4.B235

Froy, H., Phillips, R. A., Wood, A. G., Nussey, D. H., & Lewis, S. (2013). Age-related variation in reproductive traits in the wandering albatross: Evidence for terminal improvement following senescence. Ecology Letters, 16(5), 642-649. https://doi.org/10.1111/ele.12092

Froy, H., Sparks, A. M., Watt, K., Sinclair, R., Bach, F., Pilkington, J. G., Pemberton, J. M., McNeilly, T. N., & Nussey, D. H. (2019). Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science, 365(6459), 1296-1298. https://doi.org/10.1126/science.aaw5822

García, D., Smith, C., Machín, E., Loureiro, M., & Reichard, M. (2019). Changing patterns of growth in a changing planet: How a shift in phenology affects critical life-history traits in annual fishes. Freshwater Biology, 64(10), 1848-1858. https://doi.org/10.1111/fwb.13376

Grafen, A. (1988). On the uses of data on lifetime reproductive success. In T. Clutton-Brock (Ed.), Reproductive success (pp. 454-471). University of Chicago Press.

Hämäläinen, A., Dammhahn, M., Aujard, F., Eberle, M., Hardy, I., Kappeler, P. M., Perret, M., Schliehe-Diecks, S., & Kraus, C. (2014). Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate. Proceedings of the Royal Society B: Biological Sciences, 281, 20140830. https://doi.org/10.1098/rspb.2014.0830

Hamilton, W. D. (1966). The moulding of senescence by natural selection. Journal of Theoretical Biology, 12(1), 12-45. https://doi.org/10.1016/0022-5193(66)90184-6

Hayward, A. D., Wilson, A. J., Pilkington, J. G., Clutton-Brock, T. H., Pemberton, J. M., & Kruuk, L. E. B. (2013). Reproductive senescence in female Soay sheep: Variation across traits and contributions of individual ageing and selective disappearance. Functional Ecology, 27(1), 184-195. https://doi.org/10.1111/1365-2435.12029

Heath, D. D., Heath, J. W., Bryden, C. A., Johnson, R. M., & Fox, C. W. (2003). Rapid evolution of egg size in captive salmon. Science, 299(5613), 1738-1740. https://doi.org/10.1126/science.1079707

Heino, M., & Kaitala, V. (1999). Evolution of resource allocation between growth and reproduction in animals with indeterminate growth. Journal of Evolutionary Biology, 12(3), 423-429. https://doi.org/10.1046/j.1420-9101.1999.00044.x

Hu, C. K., & Brunet, A. (2018). The African turquoise killifish: A research organism to study vertebrate aging and diapause. Aging Cell, 17(3), 1-15. https://doi.org/10.1111/acel.12757

Jones, O. R., Gaillard, J.-M., Tuljapurkar, S., Alho, J. S., Armitage, K. B., Becker, P. H., Bize, P., Brommer, J., Charmantier, A., Charpentier, M., Clutton-Brock, T., Dobson, F. S., Festa-Bianchet, M., Gustafsson, L., Jensen, H., Jones, C. G., Lillandt, B.-G., McCleery, R., Merilä, J., … Coulson, T. (2008). Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecology Letters, 11(7), 664-673. https://doi.org/10.1111/j.1461-0248.2008.01187.x

Jubb, R. A. (1971). A new Nothobranchius (Pisces, Cyprinodontidae) from Southeastern Rhodesia. Journal of American Killifish Association, 8, 12-19.

Kimber, C. M., & Chippindale, A. K. (2013). Mutation, condition, and the maintenance of extended lifespan in Drosophila. Current Biology, 23(22), 2283-2287. https://doi.org/10.1016/j.cub.2013.09.049

Kirkwood, T. B. L. (1977). The evolution of aging. Nature, 270, 301-304.

Kirkwood, T. B. L., & Austad, S. N. (2000). Why do we age? Nature, 408(6809), 233-238. https://doi.org/10.1038/35041682

Kirschner, J., Weber, D., Neuschl, C., Franke, A., Böttger, M., Zielke, L., Powalsky, E., Groth, M., Shagin, D., Petzold, A., Hartmann, N., Englert, C., Brockmann, G. A., Platzer, M., Cellerino, A., & Reichwald, K. (2012). Mapping of quantitative trait loci controlling lifespan in the short-lived fish Nothobranchius furzeri-A new vertebrate model for age research. Aging Cell, 11(2), 252-261. https://doi.org/10.1111/j.1474-9726.2011.00780.x

Lemaître, J. F., & Gaillard, J. M. (2017). Reproductive senescence: New perspectives in the wild. Biological Reviews, 92(4), 2182-2199. https://doi.org/10.1111/brv.12328

Lemaitre, J. F., Ronget, V., & Gaillard, J. M. (2020). Female reproductive senescence across mammals: A high diversity of patterns modulated by life history and mating traits. Mechanisms of Ageing, 192, 111377. https://doi.org/10.1016/j.mad.2020.111377

Maklakov, A. A., Rowe, L., & Friberg, U. (2015). Why organisms age: Evolution of senescence under positive pleiotropy? BioEssays, 37(7), 802-807. https://doi.org/10.1002/bies.201500025

Mason, G. J. (2010). Species differences in response to captivity: Stress, welfare and the comparative method. Trends in Ecology & Evolution, 25(12), 713-721. https://doi.org/10.1016/j.tree.2010.08.011

Medawar, P. B. (1952). An unsolved problem in biology. Levis.

Miller, R. A., Harper, J. M., Dvsko, R. C., Durkee, S. J., & Austad, S. N. (2002). Longer life spans and delayed maturation in wild-derived mice. Experimental Biology and Medicine, 227(7), 500-508. https://doi.org/10.1177/153537020222700715

Nussey, D. H., Coulson, T., Festa-Bianchet, M., & Gaillard, J. M. (2008). Measuring senescence in wild animal populations: Towards a longitudinal approach. Functional Ecology, 22(3), 393-406. https://doi.org/10.1111/j.1365-2435.2008.01408.x

Parrish, R. H., Mallicoate, D. L., & Klingbeil, R. A. (1986). Age dependent fecundity, number of spawninge per year, sex ratio, and maturation stages in northern anchovy, Engraulis mordax. Fishery Bulletin, 84(3), 503-517.

Polačik, M., Blažek, R., & Reichard, M. (2016). Laboratory breeding of the short-lived annual killifish Nothobranchius furzeri. Nature Protocols, 11(8), 1396-1413. https://doi.org/10.1038/nprot.2016.080

Polačik, M., Blažek, R., Řežucha, R., Vrtílek, M., Terzibasi Tozzini, E., & Reichard, M. (2014). Alternative intrapopulation life-history strategies and their trade-offs in an African annual fish. Journal of Evolutionary Biology, 27(5), 854-865. https://doi.org/10.1111/jeb.12359

Preston, B. T., Saint Jalme, M., Hingrat, Y., Lacroix, F., & Sorci, G. (2015). The sperm of aging male bustards retards their offspring's development. Nature Communications, 6, 6146. https://doi.org/10.1038/ncomms7146

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., & Polačik, M. (2019). Nothobranchius furzeri, an ‘instant’ fish from an ephemeral habitat. Elife, 8, e41548. https://doi.org/10.6084/m9.fig-share.7017167

Reichard, M., Polačik, M., Blažek, R., & Vrtílek, M. (2014). Female bias in the adult sex ratio of African annual fishes: Interspecific differences, seasonal trends and environmental predictors. Evolutionary Ecology, 28(6), 1105-1120. https://doi.org/10.1007/s10682-014-9732-9

Reichwald, K., Petzold, A., Koch, P., Downie, B. R., 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, S. S., Sharma, V., Kraus, J. M., … Platzer, M. (2015). Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell, 163(6), 1527-1538. https://doi.org/10.1016/j.cell.2015.10.071

Reznick, D. N., Bryant, M. J., Roff, D., Ghalambor, C. K., & Ghalambor, D. E. (2004). Effect of extrinsic mortality on the evolution of senescence in guppies. Nature, 431(7012), 1095-1099. https://doi.org/10.1038/nature02936

Reznick, D. N., Ghalambor, C., & Nunney, L. (2002). The evolution of senescence in fish. Mechanisms of Ageing and Development, 123, 773-789. https://doi.org/10.1016/S0047-6374(01)00423-7

Ricklefs, R. E., & Cadena, C. D. (2007). Lifespan is unrelated to investment in reproduction in populations of mammals and birds in captivity. Ecology Letters, 10(10), 867-872. https://doi.org/10.1111/j.1461-0248.2007.01085.x

Ricklefs, R. E., Scheuerlein, A., & Cohen, A. (2003). Age-related patterns of fertility in captive populations of birds and mammals. Experimental Gerontology, 38(7), 741-745. https://doi.org/10.1016/S0531-5565(03)00101-3

Rose, M. R. (1984). Genetic covariation in Drosophila life history: Untangling the data. The American Naturalist, 123(4), 565-569. https://doi.org/10.1086/284222

Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1(2), 103-113. https://doi.org/10.1111/j.2041-210X.2010.00012.x

Schreibman, M. P., Margolis-Kazan, H., Bloom, J. L., & Kallman, K. D. (1983). Continued reproductive potential in aging platyfish as demonstrated by the persistence of gonadotropin, luteinizing hormone releasing hormone and spermatogenesis. Mechanisms of Ageing and Development, 22, 105-112. https://doi.org/10.1016/0047-6374(83)90103-3

Sebens, K. P. (1987). The ecology of indeterminate growth in animals. Annual Review of Ecology and Systematics, 143, 371-407. https://doi.org/10.1146/annurev.es.18.110187.002103

Service, P. M., & Rose, M. R. (1985). Genetic covariation among life-history components: The effect of novel environments. Evolution, 39(4), 943-944. https://doi.org/10.1111/j.1558-5646.1985.tb00436.x

Sgro, C. M., & Partridge, L. (2000). Evolutionary responses of the life history of wild-caught Drosophila melanogaster to two standard methods of laboratory culture. The American Naturalist, 156(4), 341-353. https://doi.org/10.1086/303394

Stearns, S. C. (1992). The evolution of life histories. Oxford University Press.

Terzibasi, E., Valenzano, D. R., Benedetti, M., Roncaglia, P., Cattaneo, A., Domenici, L., & Cellerino, A. (2008). Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS ONE, 3(12), e3866. https://doi.org/10.1371/journal.pone.0003866

Therneau, T. M., & Grambsch, P. M. (2000). Modeling survival data: Extending the Cox model. Springer.

Tidière, M., Gaillard, J.-M., Berger, V., Müller, D. W. H., Bingaman Lackey, L., Gimenez, O., Clauss, M., & Lemaître, J.-F. (2016). Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Scientific Reports, 6, 36361. https://doi.org/10.1038/srep36361

Valdesalici, S., & 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

Vaupel, J. W., Baudisch, A., Dölling, M., Roach, D. A., & Gampe, J. (2004). The case for negative senescence. Theoretical Population Biology, 65(4), 339-351. https://doi.org/10.1016/j.tpb.2003.12.003

Vrtílek, M., Žák, J., Blažek, R., Polačik, M., Cellerino, A., & Reichard, M. (2018). 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

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

Warner, D. A., Miller, D. A. W., Bronikowski, A. M., & Janzen, F. J. (2016). Decades of field data reveal that turtles senesce in the wild. Proceedings of the National Academy of Sciences of the United States of America, 113(23), 6502-6507. https://doi.org/10.1073/pnas.1600035113

Willemsen, D., Cui, R., Reichard, M., & Valenzano, D. R. (2020). Intra-species differences in population size shape life history and genome evolution. Elife, 9, e55794.

Williams, G. C. (1957). Pleiotropy, natural selection and the evolution of senescence. Evolution, 11(4), 398-411. https://doi.org/10.1111/j.1558-5646.1957.tb02911.x

Winemiller, K. O., & Rose, K. A. (1992). Patterns of life-history diversification in north American fishes: Implications for population regulation. Canadian Journal of Fisheries and Aquatic Sciences, 49(10), 2196-2218. https://doi.org/10.1139/f92-242

Wood, S. N. (2017). Generalized additive models: An introduction with R. Chapman and Hall/CRC.

Žák, J., & Reichard, M. (2020). Reproductive senescence in a short-lived fish. Figshare Repository, https://doi.org/10.6084/m9.figshare.1209596

Žák, J., Vrtílek, M., & Reichard, M. (2019). Diel schedules of locomotor, reproductive and feeding activity in wild populations of African annual killifish. Biological Journal of the Linnean Society, 182, 435-450. https://doi.org/10.1093/biolinnean/blz108

Fins as a reliable surrogate tissue for age-related changes of telomeres and DNA methylation in gonads of a short-lived fish