Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient
Status PubMed-not-MEDLINE Language English Country Great Britain, England Media electronic-ecollection
Document type Journal Article
PubMed
27547365
PubMed Central
PMC4983602
DOI
10.1002/ece3.2337
PII: ECE32337
Knihovny.cz E-resources
- Keywords
- Annual killifish, egg size, interpopulation variation, intrapopulation variability, life expectancy, reproductive allocation,
- Publication type
- Journal Article MeSH
The evolution of life history is shaped by life expectancy. Life-history traits coevolve, and optimal states for particular traits are constrained by trade-offs with other life-history traits. Life histories contrast among species, but may also diverge intraspecifically, at the level of populations. We studied the evolution of female reproductive allocation strategy, using natural populations of two sympatric species of African annual fishes, Nothobranchius furzeri and Nothobranchius orthonotus. These species inhabit pools in the Mozambican savanna that are formed in the rainy season and persist for only 2-10 months. Using 207 female N. furzeri from 11 populations and 243 female N. orthonotus from 14 populations, we tested the effects of genetic background (intraspecific lineage) and life expectancy (position on the aridity gradient determining maximum duration of their temporary habitat) on female fecundity traits. First, we found that variation in female body mass was small within populations, but varied considerably among populations. Second, we found that fecundity was largely defined by female body mass and that females spawned most of their eggs in the morning. Third, we found that the trade-off between egg size and egg number varied among lineages of N. furzeri and this outcome has been confirmed by data from two separate years. Overall, we demonstrate that local conditions were important determinants for Nothobranchius growth and fecundity and that eggs size in arid region was less limited by female fecundity than in humid region.
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Ab Ghani, N. I. , Herczeg G., and Merilä J.. 2012. Body size divergence in nine‐spined sticklebacks: disentangling additive genetic and maternal effects. Biol. J. Linn. Soc. 107:521–528.
Arendt, J. D. 1997. Adaptive intrinsic growth rates: an integration across taxa. Q. Rev. Biol. 72:149–177.
Arenzon, A. , Peret A. C., and Bohrer M. B. C.. 1999. Reproduction of the annual fish Cynopoecilus melanotaenia (Regan, 1912) in a temporary water body in Rio Grande do Sul, Brazil (Cyprinodontiformes, Rivulidae). Hydrobiologia 411:65–70. PubMed
Bartáková, V. , Reichard M., Blažek R., Polačik M., and Bryja J.. 2015. Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J. Biogeogr. 42:1832–1844.
Bartáková, V. , Reichard M., Janko K., Polačik M., Blažek R., Reichwald K., et al. 2013. Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol. Biol. 13:196. PubMed PMC
Bartoń, K. , and the R Development Core Team . 2015. MuMIn: multi‐model inference. R package version 1.15.1. Available at https://cran.r-project.org/web/packages/MuMIn/index.html.
Bernardo, J. 1996a. The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Integr. Comp. Biol. 36:216–236.
Bernardo, J. 1996b. Maternal effects in animal ecology. Am. Zool. 36:83–105.
Blanckenhorn, W. U. 2000. The evolution of body size: what keeps organisms small? Q. Rev. Biol. 75:385–407. PubMed
Blažek, R. , Polačik M., and Reichard M.. 2013. Rapid growth, early maturation and short generation time in African annual fishes. Evodevo 4:24. PubMed PMC
Bolker, B. M. , Brooks M. E., Clark C. J., Geange S. W., Poulsen J. R., Stevens M. H. H., et al. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24:127–135. PubMed
Boonekamp, J. J. , Salomons M., Bouwhuis S., Dijkstra C., and Verhulst S.. 2014. Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol. Lett. 17:599–605. PubMed
Bronikowski, A. M. 2000. Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans . Evolution 54:1760–1767. PubMed
Bryant, M. J. , and Grant J. W. A.. 1995. Resource defence, monopolization and variation of fitness in groups of female Japanese medaka depend on the synchrony of food arrival. Anim. Behav. 49:1469–1479.
Burnham, K. P. , and Anderson D. R.. 2002. Model selection and multimodel inference: a practical information‐theoretic approach. Springer, New York.
Burnham, K. P. , Anderson D. R., and Huyvaert K. P.. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65:23–35.
Cellerino, A. , Valenzano D. R., and Reichard M.. 2016. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol. Rev. 51:511–533. PubMed
Descamps, S. , Boutin S., Berteaux D., and Gaillard J.‐M.. 2006. Best squirrels trade a long life for an early reproduction. Proc. Biol. Sci. 273:2369–2374. PubMed PMC
Einum, S. , and Fleming I. A.. 1999. Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proc. Biol. Sci. 266:2095–2100.
Einum, S. , and Fleming I. A.. 2000. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 57:565–567. PubMed
Fox, C. W. , and Czesak M. E.. 2000. Evolutionary ecology of progeny size in arthropods. Annu. Rev. Entomol. 45:341–369. PubMed
Genade, T. , Benedetti M., Terzibasi E., Roncaglia P., Valenzano D. R., Cattaneo A., et al. 2005. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 4:223–233. PubMed
Grueber, C. E. , Nakagawa S., Laws R. J., and Jamieson I. G.. 2011. Multimodel inference in ecology and evolution: challenges and solutions. J. Evol. Biol. 24:699–711. PubMed
Haas, R. 1976b. Behavioral biology of the annual killifish, Nothobranchius guentheri . Copeia 1976:80–91.
Haas, R. 1976a. Sexual selection in Nothobranchius guentheri (Pisces: Cyprinodontidae). Evolution 30:614–622. PubMed
Heino, M. , and Kaitala V.. 1999. Evolution of resource allocation between growth and reproduction in animals with indeterminate growth. J. Evol. Biol. 12:423–429.
Hutchings, J. A. . 1993. Adaptive life histories effected by age‐specific survival and growth rate. Ecology 74:673–684.
Janzen, F. J. , and Warner D. A.. 2009. Parent‐offspring conflict and selection on egg size in turtles. J. Evol. Biol. 22:2222–2230. PubMed
Kindsvater, H. K. , Bonsall M. B., and Alonzo S. H.. 2011. Survival costs of reproduction predict age‐dependent variation in maternal investment. J. Evol. Biol. 24:2230–2240. PubMed
Kirkwood, T. B. L. , and Rose M. R.. 1991. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 332:15–24. PubMed
Kozłowski, J. 1992. Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7:15–19. PubMed
Lim, J. N. , Senior A. M., and Nakagawa S.. 2014. Heterogeneity in individual quality and reproductive trade‐offs within species. Evolution 68:2306–2318. PubMed
Meintjes, S. 1996. Seasonal changes in the invertebrate community of small shallow ephemeral pans at Bain's Vlei, South Africa. Hydrobiologia 317:51–64.
Messina, F. J. , and Fry J. D.. 2003. Environment‐dependent reversal of a life history trade‐off in the seed beetle Callosobruchus maculatus . J. Evol. Biol. 16:501–509. PubMed
Michod, R. E. 1979. Evolution of life histories in response to age‐specific mortality factors. Am. Nat. 113:531–550.
Morrison, C. , and Hero J.‐M.. 2003. Geographic variation in life‐history characteristics of amphibians: a review. J. Anim. Ecol. 72:270–279.
Morrongiello, J. R. , Bond N. R., Crook D. A., and Wong B. B. M.. 2012. Spatial variation in egg size and egg number reflects trade‐offs and bet‐hedging in a freshwater fish. J. Anim. Ecol. 81:806–817. PubMed
Nakagawa, S. , and Schielzeth H.. 2010. Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists. Biol. Rev. 85:935–956. PubMed
Nakagawa, S. , and Schielzeth H.. 2013. A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods Ecol. Evol. 4:133–142.
van Noordwijk, A. J. , and de Jong G.. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128:137–142.
Passos, C. , Tassino B., Rosenthal G. G., and Reichard M. 2015. Reproductive behavior and sexual selection in annual fishes Pp. 207–230 in Berois N., García G., and de Sá R., eds. Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, FA, USA. CRC Press (Boca Raton), pp. 207–230.
Pinheiro, J. , Bates D., DebRoy S., Sarkar D., and the R Development Core Team . 2015. nlme: Linear and nonlinear mixed effects models. R package version 3.1–103. Available at https://cran.r-project.org/web/packages/nlme/index.html.
Podrabsky, J. E. , and Hand S. C.. 1999. The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus . J. Exp. Biol. 202:2567–2580. PubMed
Polačik, M. , and Reichard M.. 2010. Diet overlap among three sympatric African annual killifish species Nothobranchius spp. from Mozambique. J. Fish Biol. 77:754–768. PubMed
Polačik, M. , and Reichard M.. 2011. Asymmetric reproductive isolation between two sympatric annual killifish with extremely short lifespans. PLoS One 6:e22684. PubMed PMC
Polačik, M. , Donner M. T., and Reichard M.. 2011. Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? J. Fish Biol. 78:796–809. PubMed
Polačik, M. , Harrod C., Blažek R., and Reichard M.. 2014a. Trophic niche partitioning in communities of African annual fish: evidence from stable isotopes. Hydrobiologia 721:99–106.
Polačik, M. , Blažek R., Řežucha R., et al. 2014b. Alternative intrapopulation life‐history strategies and their trade‐offs in an African annual fish. J. Evol. Biol. 27:854–865. PubMed
Polačik, M. , Blažek R., and Reichard M.. 2016. Laboratory breeding of the short‐lived annual killifish Nothobranchius furzeri . Nat. Protoc. 11:1396–1413. PubMed
Quince, C. , Shuter B. J., Abrams P. A., and Lester N. P.. 2008. Biphasic growth in fish II: empirical assessment. J. Theor. Biol. 254:197–206. PubMed
R Core Team . 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: Available at: http://www.R-project.org/.
Rasband, W. 2012. ImageJ. National Institute for Health, Bethesda, MD: Available at: http://imagej.nih.gov/ij/.
Reichard, M. , Polačik M., and Sedláček O.. 2009. Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span. J. Fish Biol. 74:198–212. PubMed
Reichard, M. , Polačik M., Blažek R., and Vrtílek M.. 2014. Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol. Ecol. 28:1105–1120.
Reznick, D. N. , Bryant M. J., Roff D. A., Ghalambor C. K., and Ghalambor D. E.. 2004. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099. PubMed
Roff, D. A. , and Fairbairn D. J.. 2007. The evolution of trade‐offs: where are we? J. Evol. Biol. 20:433–447. PubMed
Rollinson, N. , and Hutchings J. A.. 2013. The relationship between offspring size and fitness: integrating theory and empiricism. Ecology 94:315–324. PubMed
Santo, N. , Caprioli M., Orsenigo S., and Ricci C.. 2001. Egg size and offspring fitness in a bdelloid rotifer. Hydrobiologia 446:71–74.
Schielzeth, H. 2010. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1:103–113.
Sletvold, N. , and Ågren J.. 2015. Climate‐dependent costs of reproduction: survival and fecundity costs decline with length of the growing season and summer temperature. Ecol. Lett. 18:357–364. PubMed
Smith, C. C. , and Fretwell S. D.. 1974. The optimal balance between size and number of offspring. Am. Nat. 108:499–506.
Stahlschmidt, Z. R. , and Adamo S. A.. 2015. Food‐limited mothers favour offspring quality over offspring number: a principal components approach. Funct. Ecol. 29:88–95.
Stearns, S. C. 1992. The Evolution of Life Histories. Oxford Univ. Press, Oxford, U.K.
Stearns, S. C. , and Koella J. C.. 1986. The evolution of phenotypic plasticity in life‐history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893–913. PubMed
Terzibasi Tozzini, E. , Dorn A., Ng'oma E., Polačik M., Blažek R., Reichwald K., et al. 2013. Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evol. Biol. 13:77. PubMed PMC
Terzibasi, E. , Valenzano D. R., Benedetti M., Roncaglia P., Cattaneo A., Domenici L., et al. 2008. Large differences in aging phenotype between strains of the short‐lived annual fish Nothobranchius furzeri . PLoS One 3:e3866. PubMed PMC
Tibblin, P. , Forsman A., Koch‐Schmidt P., Nordahl O., Johannessen P., Nilsson J., et al. 2015. Evolutionary divergence of adult body size and juvenile growth in sympatric subpopulations of a top predator in aquatic ecosystems. Am. Nat. 186:98–110. PubMed
Trabucco, A. , and Zomer R. J.. 2009. Global Aridity Index (Global‐Aridity) and Global Potential Evapo‐Transpiration (Global‐PET) Geospatial Database. CGIAR Consortium for Spatial Information. Published online, available from the CGIAR‐CSI GeoPortal at: http://www.csi.cgiar.org/.
Uller, T. , and Olsson M.. 2005. Trade‐offs between offspring size and number in the lizard Lacerta vivipara: a comparison between field and laboratory conditions. J. Zool. 265:295–299.
Valenzano, D. R. , Singh P. P., Beyer A., Johnson E. A., and Brunet A. 2015. The African turquoise killifish genome provides insights into evolution and genetic architecture of lifespan. Cell 163:1–16. PubMed PMC
Vrtílek, M. , and Reichard M.. 2015. Highly plastic resource allocation to growth and reproduction in females of an African annual fish. Ecol. Freshw. Fish 24:616–628.
Vrtílek, M. , and Reichard M.. 2016. Patterns of morphological variation among populations of the widespread annual killifish Nothobranchius orthonotus are independent of genetic divergence and biogeography. J. Zool. Sys. Evol. Res. doi:10.1111/jzs.12134. DOI
Walsh, M. R. , and Reznick D. N.. 2008. Interactions between the direct and indirect effects of predators determine life history evolution in a killifish. Proc. Natl Acad. Sci. USA 105:594–599. PubMed PMC
Williams, G. C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am. Nat. 100:687–690.
Williams, D. D. 2006. The biology of temporary waters. Oxford Univ. Press, Oxford, U.K.
Winemiller, K. O. , and Rose K. A.. 1993. Why do most fish produce so many tiny offspring? Am. Nat. 142:585–603. PubMed
Wootton, R. J. , and Smith C.. 2015. Reproductive biology of teleost fishes. Wiley‐Blackwell, Oxford, U.K.
Wourms, J. P. 1972. The developmental biology of annual fishes III. Pre‐embryonic and embryonic diapause of variable duration in the eggs of annual fishes. J. Exp. Zool. 182:389–414. PubMed
Nothobranchius furzeri, an 'instant' fish from an ephemeral habitat