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Naturally clonal vertebrates are an untapped resource in ecology and evolution research

Abstract

Science requires replication. The development of many cloned or isogenic model organisms is a testament to this. But researchers are reluctant to use these traditional animal model systems for certain questions in evolution or ecology research, because of concerns over relevance or inbreeding. It has largely been overlooked that there are a substantial number of vertebrate species that reproduce clonally in nature. Here we highlight how use of these naturally evolved, phenotypically complex animals can push the boundaries of traditional experimental design and contribute to answering fundamental questions in the fields of ecology and evolution.

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References

  1. 1.

    Edwards, J. L. et al. Cloning adult farm animals: a review of the possibilities and problems associated with somatic cell nuclear transfer. Am. J. Reprod. Immunol. 50, 113–123 (2003).

  2. 2.

    Bolker, J. Model organisms: there’s more to life than rats and flies. Nature 491, 31–33 (2012).

  3. 3.

    Hubbs, C. L. & Hubbs, L. C. Apparent parthenogenesis in nature, in a form of fish of hybrid origin. Science 76, 628–630 (1932).

  4. 4.

    Vrijenhoek, R. C., Dawley, R. M., Cole, C. J. & Bogart, J. P. in Evolution and Ecology of Unisexual Vertebrates Vol. 466 (eds Dawley, R. M. & Bogart, J. P.) 19–23 (New York State Museum Bulletin, New York, 1989).

  5. 5.

    Neaves, W. B. & Baumann, P. Unisexual reproduction among vertebrates. Trends Genet. 27, 81–88 (2011).

  6. 6.

    Avise, J. Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence In Vertebrate Animals (Oxford Univ. Press, Oxford, 2008).

  7. 7.

    Vrijenhoek, R. C. Unisexual fish: model systems for studying ecology and evolution. Annu. Rev. Ecol. Syst. 25, 71–96 (1994).

  8. 8.

    Crews, D. in Evolution and Ecology of Unisexual Vertebrates Vol. 466 (eds Dawley, R. M. & Bogart, J. P.) 132–143 (New York State Museum Bulletin, New York, 1989).

  9. 9.

    Dawley, R. M. & Bogart, J. P. Evolution and Ecology of Unisexual Vertebrates Vol. 466 (New York State Museum Bulletin: New York, 1989).

  10. 10.

    Sinclair, E. A., Pramuk, J. B., Bezy, R. L., Crandall, K. A. & Sites, J. W. Jr. DNA evidence for nonhybrid origins of parthenogenesis in natural populations of vertebrates. Evolution 64, 1346–1357 (2010).

  11. 11.

    Warren, W. C. et al. Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nat. Ecol. Evol. 2, 669–679 (2018).

  12. 12.

    Crews, D., Grassman, M. & Lindzey, J. Behavioral facilitation of reproduction in sexual and unisexual whiptail lizards. Proc. Natl Acad. Sci. USA 83, 9547–9550 (1986).

  13. 13.

    Fujita, M. K. & Moritz, C. Origin and evolution of parthenogenetic genomes in lizards: current state and future directions. Cytogenet. Genome Res. 127, 261–272 (2009).

  14. 14.

    Schlupp, I. The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst. 36, 399–417 (2005).

  15. 15.

    Lampert, K. P. & Schartl, M. The origin and evolution of a unisexual hybrid: Poecilia formosa. Phil. Trans. R. Soc. B 363, 2901–2909 (2008).

  16. 16.

    Stöck, M., Lampert, K. P., Möller, D., Schlupp, I. & Schartl, M. Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa). Mol. Ecol. 19, 5204–5215 (2010).

  17. 17.

    Moritz, C., Donnellan, S., Adams, M. & Baverstock, P. R. The origin and evolution of parthenogenesis in Heteronotia binoei (Gekkonidae): extensive genotypic diversity among parthenogens. Evolution 43, 994–1003 (1989).

  18. 18.

    Craig, S. F., Slobodkin, L. B., Wray, G. A. & Biermann, C. H. The ‘paradox’of polyembryony: a review of the cases and a hypothesis for its evolution. Evol. Ecol. 11, 127–143 (1997).

  19. 19.

    Tatarenkov, A., Lima, S. M., Taylor, D. S. & Avise, J. C. Long-term retention of self-fertilization in a fish clade. Proc. Natl Acad. Sci. USA 106, 14456–14459 (2009).

  20. 20.

    Abbott, J. K. & Morrow, E. H. Obtaining snapshots of genetic variation using hemiclonal analysis. Trends Ecol. Evol. 26, 359–368 (2011).

  21. 21.

    Bossdorf, O., Richards, C. L. & Pigliucci, M. Epigenetics for ecologists. Ecol. Lett. 11, 106–115 (2008).

  22. 22.

    Ekblom, R. & Galindo, J. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107, 1–15 (2011).

  23. 23.

    Matz, M. V. Fantastic beasts and how to sequence them: ecological genomics for obscure model organisms. Trends Genet. 34, 121–132 (2018).

  24. 24.

    Kenkel, C. D. & Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1, 0014 (2016).

  25. 25.

    Oleksiak, M. F., Churchill, G. A. & Crawford, D. L. Variation in gene expression within and among natural populations. Nat. Genet. 32, 261–266 (2002).

  26. 26.

    Crowley, J. J. et al. Analyses of allele-specific gene expression in highly divergent mouse crosses identifies pervasive allelic imbalance. Nat. Genet. 47, 353–360 (2015).

  27. 27.

    Brenowitz, E. A. & Zakon, H. H. Emerging from the bottleneck: benefits of the comparative approach to modern neuroscience. Trends Neurosci. 38, 273–278 (2015).

  28. 28.

    Todd, E. V., Black, M. A. & Gemmell, N. J. The power and promise of RNA-seq in ecology and evolution. Mol. Ecol. 25, 1224–1241 (2016).

  29. 29.

    Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6–21 (2002).

  30. 30.

    Verhoeven, K. J. F. & Preite, V. Epigenetic variation in asexually reproducing organisms. Evolution 68, 644–655 (2014).

  31. 31.

    Kalisz, S. & Purugganan, M. D. Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol. Evol. 19, 309–314 (2004).

  32. 32.

    Oldach, M. J., Workentine, M., Matz, M. V., Fan, T. Y. & Vize, P. D. Transcriptome dynamics over a lunar month in a broadcast spawning acroporid coral. Mol. Ecol. 26, 2514–2526 (2017).

  33. 33.

    Bierbach, D., Laskowski, K. L. & Wolf, M. Behavioural individuality in clonal fish arises despite near-identical rearing conditions. Nat. Commun. 8, 15361 (2017).

  34. 34.

    Edenbrow, M. & Croft, D. P. Behavioural types and life history strategies during ontogeny in the mangrove killifish. Kryptolebias marmoratus. Anim. Behav. 82, 731–741 (2011).

  35. 35.

    Schlosser, I. J., Doeringsfeld, M. R., Elder, J. F. & Arzayus, L. F. Niche relationships of clonal and sexual fish in a heterogeneous landscape. Ecology 79, 953–968 (1998).

  36. 36.

    Cole, C. J., Taylor, H. L. & Townsend, C. R. Morphological variation in a unisexual whiptail lizard (Aspidoscelis exsanguis) and one of its bisexual parental species (Aspidoscelis inornata) (Reptilia: Squamata: Teiidae): is the clonal species less variable? Am. Mus. Novit. 3849, 1–20 (2016).

  37. 37.

    Dawley, R. M., Schultz, R. J. & Goddard, K. A. Clonal reproduction and polyploidy in unisexual hybrids of Phoxinus eos and Phoxinus neogaeus (Pisces; Cyprinidae). Copeia 1987, 275–283 (1987).

  38. 38.

    Massicotte, R., Whitelaw, E. & Angers, B. DNA methylation: a source of random variation in natural populations. Epigenetics 6, 421–427 (2011).

  39. 39.

    Massicotte, R. & Angers, B. General-purpose genotype or how epigenetics extend the flexibility of a genotype. Genet. Res. Int. 2012, 317175 (2012).

  40. 40.

    Leung, C., Breton, S. & Angers, B. Facing environmental predictability with different sources of epigenetic variation. Ecol. Evol. 6, 5234–5245 (2016).

  41. 41.

    Schlupp, I., Parzefall, J. & Schartl, M. Biogeography of the Amazon molly. Poecilia formosa. J. Biogeogr. 29, 1–6 (2002).

  42. 42.

    Bi, K. & Bogart, J. P. Time and time again: unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates. BMC Evol. Biol. 10, 238 (2010).

  43. 43.

    Castonguay, E. & Angers, B. The key role of epigenetics in the persistence of asexual lineages. Genet. Res. Int. 2012, 534289 (2012).

  44. 44.

    Vogt, G. Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environ. Epigenet. 3, dvx002 (2017).

  45. 45.

    McNamara, J. M., Dall, S. R. X., Hammerstein, P. & Leimar, O. Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments. Ecol. Lett. 19, 1267–1276 (2016).

  46. 46.

    Stamps, J. A. & Frankenhuis, W. E. Bayesian models of development. Trends Ecol. Evol. 31, 260–268 (2016).

  47. 47.

    Dall, S. R., McNamara, J. M. & Leimar, O. Genes as cues: phenotypic integration of genetic and epigenetic information from a Darwinian perspective. Trends Ecol. Evol. 30, 327–333 (2015).

  48. 48.

    Mackay, T. F. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303–339 (2001).

  49. 49.

    Fisher, D. N., Brachmann, M. & Burant, J. B. Complex dynamics and the development of behavioural individuality. Anim. Behav. 138, e1–e6 (2018).

  50. 50.

    Frankenhuis, W. E. & Panchanathan, K. Balancing sampling and specialization: an adaptationist model of incremental development. Proc. R. Soc. B 278, 3558–3565 (2011).

  51. 51.

    Freund, J. et al. Emergence of individuality in genetically identical mice. Science 340, 756–759 (2013).

  52. 52.

    Vogt, G. et al. Production of different phenotypes from the same genotype in the same environment by developmental variation. J. Exp. Biol. 211, 510–523 (2008).

  53. 53.

    Gärtner, K. A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Lab. Anim. 24, 71–77 (1990).

  54. 54.

    McNamara, J. M., Green, R. F. & Olsson, O. Bayes’ theorem and its applications in animal behaviour. Oikos 112, 243–251 (2006).

  55. 55.

    Trimmer, P. C. et al. Decision-making under uncertainty: biases and Bayesians. Anim. Cogn. 14, 465–476 (2011).

  56. 56.

    Stein, L. R., Bukhari, S. A. & Bell, A. M. Personal and transgenerational cues are nonadditive at the phenotypic and molecular level. Nat. Ecol. Evol. 2, 1306–1311 (2018).

  57. 57.

    Stamps, J. A., Biro, P. A., Mitchell, D. J. & Saltz, J. B. Bayesian updating during development predicts genotypic differences in plasticity. Evolution 72, 2167–2180 (2018).

  58. 58.

    Mousseau, T. A. & Fox, C. W. The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403–407 (1998).

  59. 59.

    Weaver, I. C. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854 (2004).

  60. 60.

    Dingemanse, N. J. & Wolf, M. Recent models for adaptive personality differences: a review. Phil. Trans. R. Soc. B 365, 3947–3958 (2010).

  61. 61.

    Bolnick, D. I. et al. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).

  62. 62.

    Toscano, B. J., Gownaris, N. J., Heerhartz, S. M. & Monaco, C. J. Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecologia 182, 55–69 (2016).

  63. 63.

    Thornton, A. & Lukas, D. Individual variation in cognitive performance: developmental and evolutionary perspectives. Phil. Trans. R. Soc. B 367, 2773–2783 (2012).

  64. 64.

    Dingemanse, N. J. et al. Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J. Anim. Ecol. 76, 1128–1138 (2007).

  65. 65.

    Bell, A. M. & Sih, A. Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol. Lett. 10, 828–834 (2007).

  66. 66.

    Laskowski, K. L. & Bell, A. M. Competition avoidance drives individual differences in response to a changing food resource in sticklebacks. Ecol. Lett. 16, 746–753 (2013).

  67. 67.

    Laskowski, K. L. & Pruitt, J. N. Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider. Proc. R. Soc. B 281, 20133166 (2014).

  68. 68.

    Stamps, J. A. & Krishnan, V. V. Combining information from ancestors and personal experiences to predict individual differences in developmental trajectories. Am. Nat. 184, 647–657 (2014).

  69. 69.

    Dall, S. R. X., Houston, A. I. & McNamara, J. M. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7, 734–739 (2004).

  70. 70.

    Biro, P. A. & Stamps, J. A. Are animal personality traits linked to life-history productivity? Trends Ecol. Evol. 23, 361–368 (2008).

  71. 71.

    Wolf, M. & Weissing, F. J. An explanatory framework for adaptive personality differences. Phil. Trans. R. Soc. B 365, 3959–3968 (2010).

  72. 72.

    Edenbrow, M. & Croft, D. P. Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus. Oikos 122, 667–681 (2012).

  73. 73.

    Bijleveld, A. I. et al. Personality drives physiological adjustments and is not related to survival. Proc. R. Soc. B 281, 20133135 (2014).

  74. 74.

    Clark, C. W. Antipredator behavior and the asset-protection principle. Behav. Ecol. 5, 159–170 (1994).

  75. 75.

    Wolf, M., van Doorn, G. S., Leimar, O. & Weissing, F. J. Life-history trade-offs favour the evolution of animal personalities. Nature 447, 581–584 (2007).

  76. 76.

    Luttbeg, B. & Sih, A. Risk, resources and state-dependent adaptive behavioural syndromes. Phil. Trans. R. Soc. B 365, 3977–3990 (2010).

  77. 77.

    Mathot, K. J. & Dall, S. R. Metabolic rates can drive individual differences in information and insurance use under the risk of starvation. Am. Nat. 182, 611–620 (2013).

  78. 78.

    Kurvers, R. H. J. M., Krause, J., Croft, D. P., Wilson, A. D. M. & Wolf, M. The evolutionary and ecological consequences of animal social networks: emerging issues. Trends Ecol. Evol. 29, 326–335 (2014).

  79. 79.

    Krause, J. & Ruxton, G. D. Living in Groups (Oxford Univ. Press, Oxford, 2002).

  80. 80.

    Farine, D. R. & Whitehead, H. Constructing, conducting and interpreting animal social network analysis. J. Anim. Ecol. 84, 1144–1163 (2015).

  81. 81.

    Wolf, M. & Krause, J. Why personality differences matter for social functioning and social structure. Trends Ecol. Evol. 29, 306–308 (2014).

  82. 82.

    Laskowski, K. L., Wolf, M. & Bierbach, D. The making of winners (and losers): how early dominance interactions determine adult social structure in a clonal fish. Proc. R. Soc. B 283, 20160183 (2016).

  83. 83.

    Firth, J. A. & Sheldon, B. C. Experimental manipulation of avian social structure reveals segregation is carried over across contexts. Proc. R. Soc. B 282, 20142350 (2015).

  84. 84.

    Liker, A. & Bókony, V. Larger groups are more successful in innovative problem solving in house sparrows. Proc. Natl Acad. Sci. USA 106, 7893–7898 (2009).

  85. 85.

    Aplin, L. M. et al. Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518, 538–541 (2015).

  86. 86.

    Costa, G. C. & Schlupp, I. Biogeography of the Amazon molly: ecological niche and range limits of an asexual hybrid species. Glob. Ecol. Biogeogr. 19, 442–451 (2010).

  87. 87.

    Schultz, R. J. in Evolution and Genetics of Life Histories 103–119 (Springer, New York, 1982).

  88. 88.

    Quattro, J. M., Avise, J. C. & Vrijenhoek, R. C. An ancient clonal lineage in the fish genus Poeciliopsis (Atheriniformes: Poeciliidae). Proc. Natl Acad. Sci. USA 89, 348–352 (1992).

  89. 89.

    Bohlen, J. & Ráb, P. Species and hybrid richness in spined loaches of the genus Cobitis (Teleostei: Cobitidae), with a checklist of European forms and suggestions for conservation. J. Fish Biol. 59, 75–89 (2001).

  90. 90.

    Janko, K. et al. Diversity of European spined loaches (genus Cobitis L.): an update of the geographic distribution of the Cobitis taenia hybrid complex with a description of new molecular tools for species and hybrid determination. J. Fish Biol. 71, 387–408 (2007).

  91. 91.

    Choleva, L., Apostolou, A., Rab, P. & Janko, K. Making it on their own: sperm-dependent hybrid fishes (Cobitis) switch the sexual hosts and expand beyond the ranges of their original sperm donors. Phil. Trans. R. Soc. B 363, 2911–2919 (2008).

  92. 92.

    Bogart, J. P., Bi, K., Fu, J., Noble, D. W. & Niedzwiecki, J. Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome 50, 119–136 (2007).

  93. 93.

    Berger, L. in The Reproductive Biology of Amphibians 367–388 (Springer, New York, 1977).

  94. 94.

    Graf, J.-D. & Polls Pelaz, M. in Evolution and Ecology of Unisexual Vertebrates Vol. 466 (eds Dawley, R. M. & Bogart, J. P.) 289–301 (New York State Museum Bulletin, New York, 1989).

  95. 95.

    Taylor, H. L., Cole, C. J., Dessauer, H. C. & Parker, E. Jr. Congruent patterns of genetic and morphological variation in the parthenogenetic lizard Aspidoscelis tesselata (Squamata: Teiidae) and the origins of color pattern classes and genotypic clones in eastern New Mexico. Am. Mus. Novit. 3424, 1–40 (2003).

  96. 96.

    Dessauer, H. C. & Cole, C. J. Evolution and Ecology of Unisexual Vertebrates Vol. 466 (eds Dawley, R. M. & Bogart, J. P.) 49–71 (New York State Museum Bulletin, New York, 1989).

  97. 97.

    Moritz, C. et al. The material ancestry and approximate age of parthenogenetic species of Caucasian rock lizards (Lacerta: Lacertidae). Genetica 87, 53–62 (1992).

  98. 98.

    Uzzell, T. & Darevsky, I. S. Biochemical evidence for the hybrid origin of the parthenogenetic species of the Lacerta saxicola complex (Sauria: Lacertidae), with a discussion of some ecological and evolutionary implications. Copeia 1975, 204–222 (1975).

  99. 99.

    Reeder, T. W., Cole, C. J. & Dessauer, H. C. Phylogenetic relationships of whiptail lizards of the genus Cnemidophorus (Squamata: Teiidae): a test of monophyly, reevaluation of karyotypic evolution, and review of hybrid origins. Am. Mus. Novit. 3365, 1–61 (2002).

  100. 100.

    Tucker, D. B. et al. Methodological congruence in phylogenomic analyses with morphological support for teiid lizards (Sauria: Teiidae). Mol. Phylogenet. Evol. 103, 75–84 (2016).

  101. 101.

    Moritz, C. et al. in Evolution and Ecology of Unisexual Vertebrates Vol. 466 (eds Dawley, R. M. & Bogart, J. P.) 87–112 (New York State Museum Bulletin, New York, 1989).

  102. 102.

    Good, D. & Wright, J. Allozymes and the hybrid origin of the parthenogenetic lizard Cnemidophorus exsanguis. Experientia 40, 1012–1014 (1984).

  103. 103.

    Lutes, A. A., Baumann, D. P., Neaves, W. B. & Baumann, P. Laboratory synthesis of an independently reproducing vertebrate species. Proc. Natl Acad. Sci. USA 108, 9910–9915 (2011).

  104. 104.

    Scharnweber, K., Plath, M., Winemiller, K. O. & Tobler, M. Dietary niche overlap in sympatric asexual and sexual livebearing fishes Poecilia spp. J. Fish Biol. 79, 1760–1773 (2011).

  105. 105.

    Tobler, M. & Schlupp, I. Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the Red Queen? Biol. Lett. 1, 166–168 (2005).

  106. 106.

    Schlupp, I., Marler, C. & Ryan, M. J. Benefit to male sailfin mollies of mating with heterospecific females. Science 263, 373–374 (1994).

  107. 107.

    Vrijenhoek, R. C. Animal clones and diversity. Bioscience 48, 617–628 (1998).

  108. 108.

    Quattro, J. M., Avise, J. C. & Vrijenhoek, R. C. Molecular evidence for multiple origins of hybridogenetic fish clones (Poeciliidae:Poeciliopsis). Genetics 127, 391–398 (1991).

  109. 109.

    Vrijenhoek, R. in Population Biology and Evolution 217–231 (Springer, New York, 1984).

  110. 110.

    Gray, M. M. & Weeks, S. C. Niche breadth in clonal and sexual fish (Poeciliopsis): a test of the frozen niche variation model. Can. J. Fish. Aquat. Sci. 58, 1313–1318 (2001).

  111. 111.

    Semlitsch, R. D., Hotz, H. & Guex, G. D. Competition among tadpoles of coexisting hemiclones of hybridogenetic Rana esculenta: support for the frozen niche variation model. Evolution 51, 1249–1261 (1997).

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Acknowledgements

We thank M. Schartl and I. Schlupp for constructive conversations. This work was supported in part by the Deutsche Forschungsgemeinschaft (Grant LA 3778/1-1 to K.L.L.; grant BI 1828/2-1 to D.B.) and the Alexander von Humboldt Foundation (Postdoctoral Fellowship to C.D.).

Author information

K.L.L., M.W. and J.K. conceived the idea for the manuscript. K.L.L. wrote the initial draft. All authors substantially contributed to revisions and editing of manuscript.

Competing interests

The authors declare no competing interests.

Correspondence to Kate L. Laskowski.

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Fig. 1: Three examples of unisexual vertebrates.
Fig. 2: Modes of unisexual reproduction.