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Sex change as a survival strategy

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Abstract

Sequential hermaphroditism (sex change) is understood to be a strategy that maximizes lifetime reproduction in systems where one sex confers highest fitness early in life, and the other later in life. This strategy is evolutionarily stable despite costs to growth, survival, or current reproduction. Few studies have examined advantages of sex change outside of reproduction. The mangrove rivulus fish, Kryptolebias marmoratus, presents a unique system in which to study non-reproductive consequences of sex change because reproductive opportunity decreases significantly with sex change. In natural conditions, individuals develop as self-fertilizing simultaneous hermaphrodites. Some individuals change sex to male at various points after sexual maturity, even in isolation, essentially foregoing future reproductive assurance. In a large-scale experiment that examined fitness differences among individuals exposed to ecologically relevant environmental challenges, we found that individuals that change sex from hermaphrodite to male had overwhelmingly greater chances of survival compared to those that remained hermaphrodite. Furthermore, hermaphrodites derived from lineages with higher propensities to change sex experienced greater survival advantages by changing sex. Our results indicate that sex change may be a survival strategy, one with genotype-dependent consequences.

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References

  • Aldenhoven JM (1986) Different reproductive strategies in a sex-changing coral reef fish Centropyge bicolor (Pomacanthidae). Mar Freshw Res 37:353–360

    Google Scholar 

  • Allsop DJ, West SA (2003) Life history: changing sex at the same relative body size. Nature 425:783–784

    CAS  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Bauer G (1987) Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J Anim Ecol 56:691–704

    Google Scholar 

  • Breitburg DL (1986) Effect of variability in recruitment on selection for protogynous sex change. Am Nat 128:551–560

    Google Scholar 

  • Brooks M, Iwasa Y (2010) Size-dependent sex change can be the ESS without any size advantage of reproduction when mortality is size-dependent. Theor Popul Biol 78:183–191

    PubMed  Google Scholar 

  • Buston PM, Munday PL, Warner RR (2004) Evolutionary biology—sex change and relative body size in animals. Nature 428:U1

    Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Charnov EL (1986) Size advantage may not always favor sex change. J Theor Biol 119:283–285

    CAS  PubMed  Google Scholar 

  • Charnov EL (1987) On sex allocation and selfing in higher plants. Evol Ecol 1:30–36

    Google Scholar 

  • Charnov EL, Anderson PJ (1989) Sex change and population fluctuations in pandalid shrimp. Am Nat 134:824–827

    Google Scholar 

  • Charnov EL, Skúladóttir U (2000) Dimensionless invariants for the optimal size (age) of sex change. Evol Ecol Res 2:1067–1071

    Google Scholar 

  • Clifton KE, Rogers L (2008) Sex-specific mortality explains non-sex-change by large female Sparisoma radians. Anim Behav 75:1–10

    Google Scholar 

  • Cole KS, Noakes DLG (1997) Gonadal development and sexual allocation in mangrove killifish, Rivulus marmoratus (Pisces: Atherinomorpha). Copeia 1997:596–600

    Google Scholar 

  • Davis WP (1990) Field observations of the ecology and habits of mangrove rivulus. Ichthyol Explor Freshw 1:123–134

    Google Scholar 

  • Earley RL, Hanninen AF, Fuller A, Garcia MJ, Lee EA (2012) Phenotypic plasticity and integration in the mangrove rivulus (Kryptolebias marmoratus): a prospectus. Integr Comp Biol 52:814–827

    PubMed  PubMed Central  Google Scholar 

  • Ellison A, Cable J, Consuegra S (2011) Best of both worlds? association between outcrossing and parasite loads in a selfing fish. Evolution 65:3021–3026

    PubMed  Google Scholar 

  • Ellison A, Wright P, Taylor DS, Cooper C, Regan K, Currie S, Consuegra S (2012) Environmental diel variation, parasite loads, and local population structuring of a mixed-mating mangrove fish. Ecol Evolut 2:1682–1695

    Google Scholar 

  • Ellison A, De Leaniz CG, Consuegra S (2013) Inbred and furious: negative association between aggression and genetic diversity in highly inbred fish. Mol Ecol 22:2292–2300

    PubMed  Google Scholar 

  • Ellison A, Rodrı CM, Moran P, Breen J, Swain M, Megias M, Hegarty M et al (2015) Epigenetic regulation of sex ratios may explain natural variation in self-fertilization rates. Proc R Soc B 282:20151900

    PubMed  Google Scholar 

  • Fisher RF (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks

    Google Scholar 

  • Freeman DC, Harper KT, Charnov EL (1980) Sex change in plants: old and new observations and new hypotheses. Oecologia 47:222–232

    CAS  PubMed  Google Scholar 

  • Furness AI, Tatarenkov A, Avise JC (2015) A genetic test for whether pairs of hermaphrodites can cross-fertilize in a selfing killifish. J Hered 106:749–752

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208

    CAS  PubMed  Google Scholar 

  • Guide for the care and use of laboratory animals (2010) National Academies Press

  • Harrington RW Jr (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134:1749–1750

    PubMed  Google Scholar 

  • Harrington RW Jr (1963) Twenty-four-hour rhythms of internal self-fertilization and of oviposition by hermaphrodites of Rivulus marmoratus. Physiol Zool 36:325–341

    Google Scholar 

  • Harrington RW Jr (1967) Environmentally controlled induction of primary male gonochorists from eggs of the self- fertilizing hermaphroditic fish, Rivulus marmoratus Poey. Biol Bull 132:174–199

    PubMed  Google Scholar 

  • Harrington RW Jr (1971) How ecological and genetic factors interact to determine when self-fertlizing hermaphrodites of Rivulus marmoratus change into functional secondary males, with a reappraisal of the modes of intersexuality among fishes. Copeia 1971:389–432

    Google Scholar 

  • Harrington RW Jr (1975) Sex setermination and differentiation among uniparental homozygotes of the hermaphroditic fish Rivulus marmoratus (Cyprinodontidae: Atheriniformes). In: Reinboth R (ed) Intersexuality in the animal Kingdom. Springer, Berlin, pp 249–262

    Google Scholar 

  • Harrington RW Jr, Rivas L (1958) The discovery in Florida of the cyprinodont fish, Rivulus marmoratus, with a redescription and ecological notes. Copeia 1958:125–130

    Google Scholar 

  • Hoch JM, Cahill AE (2012) Variation in size at sex-change among natural populations of the protandrous hermaphrodite, Crepidula fornicata (Gastropoda, Calyptraeidae). Mar Biol 159:897–905

    Google Scholar 

  • Hoffman SG, Schildhauer MP, Warner RR (1985) The costs of changing sex and the ontogeny of males under contest competition for mates. Evolution 39:915–927

    PubMed  Google Scholar 

  • Iwasa Y (1991) Sex change evolution and cost of reproduction. Behav Ecol 2:56–68

    Google Scholar 

  • JMP®, Version 14 Pro. 2019. SAS Institute Inc., Cary

  • Kazancıoğlu E, Alonzo SH (2009) Costs of changing sex do not explain why sequential hermaphroditism is rare. Am Nat 173:327–336

    PubMed  Google Scholar 

  • Leigh EG, Charnov EL, Warner RR (1976) Sex ratio, sex change, and natural selection. Proc Natl Acad Sci 73:3656–3660

    PubMed  Google Scholar 

  • Lenth R (2019) emmeans: estimated marginal means, aka least-squares means. R package, version 1.3.2. https://CRAN.R-project.org/package=emmeans

  • Lomax JL, Carlson RE, Wells JW, Crawford PM, Earley RL (2017) Factors affecting egg production in the selfing mangrove rivulus (Kryptolebias marmoratus). Zoology 122:38–45

    PubMed  Google Scholar 

  • Luke KN, Bechler DL (2010) The role of dyadic interactions in the mixed-mating strategies of the mangrove rivulus Kryptolebias marmoratus. Curr Zool 56:6–17

    Google Scholar 

  • Mackiewicz M, Tatarenkov A, Perry A, Martin JR, Elder JF, Bechler DL, Avise JC (2006) Microsatellite documentation of male-mediated outcrossing between inbred laboratory strains of the self-fertilizing mangrove killifish (Kryptolebias marmoratus). J Hered 97:508–513

    CAS  PubMed  Google Scholar 

  • Marson KM, Taylor DS, Earley RL (2019) Cryptic male phenotypes in the mangrove rivulus fish, Kryptolebias marmoratus. Biol Bull 236:13–28

    PubMed  Google Scholar 

  • Martin SB (2007) Association behaviour of the self-fertilizing Kryptolebias marmoratus (Poey): The influence of microhabitat use on the potential for a complex mating system. J Fish Biol 71:1383–1392

    Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge Univ Press, Cambridge

    Google Scholar 

  • Molloy PP, Nyboer EA, Côté IM (2011) Male-male competition in a mixed-mating fish. Ethology 117:586–596

    Google Scholar 

  • Munday PL, Molony BW (2002) The energetic cost of protogynous versus protandrous sex change in the bi-directional sex-changing fish Gobiodon histrio. Mar Biol 141:1011–1017

    CAS  Google Scholar 

  • Munday PL, Buston PM, Warner RR (2006a) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21:89–95

    PubMed  Google Scholar 

  • Munday PL, Wilson White J, Warner RR (2006b) A social basis for the development of primary males in a sex-changing fish. Proc R Soc B Biol Sci 273:2845–2851

    Google Scholar 

  • Nakamura Y, Suga K, Sakakura Y, Sakamoto T, Hagiwara A (2008) Genetic and growth differences in the outcrossings between two clonal strains of the self-fertilizing mangrove killifish. Can J Zool 86:976–982

    Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rodgers EW, Earley RL, Grober MS (2007) Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. J Fish Biol 70:1660–1668

    Google Scholar 

  • RStudioTeam (2016) RStudio: integrated development for R. RStudio Inc, Boston

    Google Scholar 

  • Sakakura Y, Soyano K, Noakes DLG, Hagiwara A (2006) Gonadal morphology in the self-fertilizing mangrove killifish, Kryptolebias marmoratus. Ichthyol Res 53:427–430

    Google Scholar 

  • Scarsella GE, Gresham JD, Earley RL (2018) Relationships between external sexually dimorphic characteristics and internal gonadal morphology in a sex-changing fish. J Zool 305:133–140

    Google Scholar 

  • Tatarenkov A, Gao H, Mackiewicz M, Taylor DS, Turner BJ, Avise JC (2007) Strong population structure despite evidence of recent migration in a selfing hermaphroditic vertebrate, the mangrove killifish (Kryptolebias marmoratus). Mol Ecol 16:2701–2711

    PubMed  Google Scholar 

  • Tatarenkov A, Lima SMQ, Earley RL, Berbel-Filho WM, Vermeulen FBM, Taylor DS, Marson K et al (2017) Deep and concordant subdivisions in the self-fertilizing mangrove killifishes (Kryptolebias) revealed by nuclear and mtDNA markers. Biol J Lin Soc 122:558–578

    Google Scholar 

  • Taylor DS (2012) Twenty-four years in the mud: What have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebias marmoratus? Integr Comp Biol 52:724–736

    PubMed  PubMed Central  Google Scholar 

  • Taylor DS, Turner BJ, Davis WP, Chapman BB (2008) A novel terrestrial fish habitat inside emergent logs. Am Nat 171:263–266

    PubMed  Google Scholar 

  • Todd EV, Ortega-Recalde O, Liu H, Lamm MS, Rutherford KM, Cross H, Black MA et al (2019) Stress, novel sex genes and epigenetic reprogramming orchestrate socially-controlled sex change. Sci Adv 5:eaaw7006

    PubMed  PubMed Central  Google Scholar 

  • Turner BJ, Fisher MT, Taylor DS, Davis WP, Jarrett BL (2006) Evolution of “maleness” and outcrossing in a population of the self-fertilizing killifish, Kryptolebias marmoratus. Evol Ecol Res 8:1475–1486

    Google Scholar 

  • Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109:61–82

    Google Scholar 

  • Warner RR (1988a) Sex change in fishes: hypotheses, evidence, and objections. Environ Biol Fishes 22:81–90

    Google Scholar 

  • Warner RR (1988b) Sex change and the size-advantage model. Trends Ecol Evol 3:133–136

    CAS  PubMed  Google Scholar 

  • Warner RR, Robertson DR, Leigh EG (1975) Sex change and sexual selection. Science 190:633–638

    CAS  PubMed  Google Scholar 

  • Yamaguchi S (2016) Time required for sex change in teleost fishes: hormonal dynamics shaped by selection. J Theor Biol 407:339–348

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to two anonymous reviewers and an editor for valuable comments that significantly improved the manuscript. This work was supported by E. O. Wilson Fellowship (University of Alabama), Edward C. Raney Fund (American Society of Ichthyologists and Herpetologists), Graduate Council Fellowship (University of Alabama), and Research Grants Committee (University of California, Irvine). All procedures were approved by the University of Alabama Institutional Animal Care and Use Committee (protocols #13-10-0048 and #15-04-0102). Field activities, including collection methods and processing of animals, were approved by a Florida Fish and Wildlife Conservation Commission Special Activity License (SAL-15-1132A-SR), Florida Department of Environmental Protection State Park permits (06051410, 06261510, and 06231610), a Brevard County Environmentally Endangered Lands Program Research permit, and a Pinellas County Parks and Conservation Resources research permit.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Alabama, 300 Hackberry Lane, Box 870344, Tuscaloosa, AL, 35487, USA

    Jennifer D. Gresham, Kristine M. Marson & Ryan L. Earley

  2. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA

    Andrey Tatarenkov

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  1. Jennifer D. Gresham
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  2. Kristine M. Marson
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  3. Andrey Tatarenkov
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Correspondence to Jennifer D. Gresham.

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Electronic supplementary material

Online appendix (as one document) includes: Study organism, Experimental design, Seasonal variation in sex change, Relationship between sex change and fecundity, Identifying males, and Extended statistical model output. Below is the link to the electronic supplementary material.

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Gresham, J.D., Marson, K.M., Tatarenkov, A. et al. Sex change as a survival strategy. Evol Ecol 34, 27–40 (2020). https://doi.org/10.1007/s10682-019-10023-2

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