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Relative size underlies alternative morph development in a salamander

  • Behavioral ecology –original research
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Abstract

Size thresholds commonly underlie the induction of alternative morphological states. However, the respective importance of absolute and relative size to such thresholds remains uncertain. If absolute size governs expression, morph frequency should differ among environments that influence absolute sizes (e.g. resources, competition), and individuals of the same morph should have similar average sizes across environments. If relative size determines expression, the frequency of each morph may not differ among environments, but morphs within each environment should differ in size relative to one another. We tested these predictions in a salamander (Ambystoma talpoideum) that develops into either a terrestrial metamorph or an aquatic paedomorph. To generate size variation within and among environments, we reared individuals in mesocosm ponds across three conspecific densities. We found that morph frequency did not differ among density treatments, and the morphs were not similarly sized within each density treatment. Instead, within each environment, relatively larger individuals became metamorphs and relatively smaller individuals became paedomorphs. Relative size therefore determined morph development, highlighting the importance of an individual’s social context to size-dependent morph induction.

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Data availability

Data used in these analyses available at Dryad Digital Repository (https://doi.org/10.5061/dryad.sf7m0cg3p)

References

  • Álvarez D, Nicieza AG (2002) Effects of temperature and food quality on anuran larval growth and metamorphosis. Funct Ecol 16:640–648

    Google Scholar 

  • Anderson TL, Whiteman HH (2015) Asymmetric effects of intra- and inter-specific competition on a pond-breeding salamander. Ecology 96:1681–1690

    Google Scholar 

  • Anderson TL, Mott CL, Levine TD, Whiteman HH (2013) Life cycle complexity influences intraguild predation and cannibalism in pond communities. Copeia 2013:284–291

    Google Scholar 

  • Anderson TL, Mott CL, Hartman BA, Whiteman HH (2018) Biotic and abiotic predictors of larval salamander size and density. Copeia 105:237–248

    Google Scholar 

  • Asquith CM, Vonesh JR (2010) Effects of size and size structure on predation and inter-cohort competition in red-eyed treefrog tadpoles. Oecologia 170:629–639

    Google Scholar 

  • Bartoń K (2019) MuMIn: multi-model inference. R package version 1(43):6

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using lme4. J Stat Softw 67:148

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Buston PM (2003) Size and growth modification in clownfish. Nature 424:145–146

    CAS  PubMed  Google Scholar 

  • Chapman BB, Brönmark C, Nilsson J-Å, Hansson L-A (2011) The ecology and evolution of partial migration. Oikos 120:1764–1775

    Google Scholar 

  • Collin R (2006) Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60:735–745

    PubMed  Google Scholar 

  • Cook CDK (1968) Phenotypic plasticity with particular reference to three amphibious plant species. In: Heywood V (ed) Modern methods in plant taxonomy. Academic Press, London, pp 97–111

    Google Scholar 

  • Denoël M, Joly P, Whiteman HH (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev 80:663–671

    PubMed  Google Scholar 

  • Denver RJ (2009) Stress hormones mediate environment-genotype interactions during amphibian development. Gen Comp Endocr 164:20–31

    CAS  PubMed  Google Scholar 

  • Development Core Team R (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dodd CK (2010) Amphibian ecology and conservation: a handbook of techniques. Oxford University Press, Oxford

    Google Scholar 

  • Doyle JM, Whiteman HH (2008) Paedomorphosis in Ambystoma talpoideum: effects of initial body size variation and density. Oecologia 156:87–94

    PubMed  Google Scholar 

  • Emlen DJ, Nijhout HF (2000) The development and evolution of exaggerated morphologies in insects. Annu Rev Entomol 45:661–708

    CAS  PubMed  Google Scholar 

  • Frankino WA, Pfennig DW (2001) Condition-dependent expression of trophic polyphenism: effects of individual size and competitive ability. Evol Ecol Res 3:939–951

    Google Scholar 

  • Freckleton RP (2011) Dealing with collinearity in behavioral and ecological data: model averaging and the problems of measurement error. Behav Ecol Sociobiol 65:91–101

    Google Scholar 

  • Gerhardt HC, Daniel RE, Perrill SA, Schramm S (1987) Mating behaviour and male mating success in the green treefrog. Anim Behav 35:1490–1503

    Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:2–98

    Google Scholar 

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711

    CAS  PubMed  Google Scholar 

  • Johnson EB, Beirzychudek P, Whiteman HH (2003) Potential of prey size and type to affect foraging asymmetries in tiger salamander (Ambystoma tigrinum nebulosum) larvae. Can J Zool 81:1726–1735

    Google Scholar 

  • Lackey ACR, Moore MP, Doyle J, Gerlanc N, Hagan A, Geile M, Eden C, Whiteman HH (2019) Lifetime fitness, sex-specific life history, and the maintenance of a polyphenism. Am Nat 194:230–245

    PubMed  Google Scholar 

  • Lenth RV (2016) Least-squares means: the R Package lsmeans. J Stat Soft 69:1–33

    Google Scholar 

  • Lorenzi V, Earley RL, Grober MS (2012) Differential responses of brain, gonad and muscle steroid levels to changes in social status and sex in a sequential and bidirectional hermaphroditic fish. PLoS ONE 7:e51158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maret TJ, Collins JP (1994) Individual responses to population size structure: the role of size expression of a trophic polyphenism. Oecologia 100:279–285

    CAS  PubMed  Google Scholar 

  • Michalczyk Ł, Dudziak M, Radwan J, Tomkins JL (2018) Fitness consequences of threshold trait expression subject to environmental cues. Proc R Soc B 285:20180783

    PubMed  Google Scholar 

  • Moczek AP, Nijhout HF (2003) Rapid evolution of polyphenic threshold. Evol Dev 5:259–268

    PubMed  Google Scholar 

  • Moczek AP, Sultan S, Foster S, Ledón-Rettig C, Dworkin I, Nijhout HF et al (2011) The role of developmental plasticity in evolutionary innovation. Proc R Soc B 278:2705–2713

    PubMed  Google Scholar 

  • Moore MP, Martin RA (2019) On the evolution of carry-over effects. J Anim Ecol 88:1832–1844

    PubMed  Google Scholar 

  • Moore MP, Whiteman HH (2016) Natal philopatry varies with larval condition in salamanders. Behav Ecol Sociobiol 70:1247–1255

    Google Scholar 

  • Moore MP, Landberg T, Whiteman HH (2015) Maternal investment mediates offspring life history variation with context-dependent fitness consequences. Ecology 96:2499–2509

    PubMed  Google Scholar 

  • Moore MP, Whiteman HH, Martin RA (2019) A mother’s legacy: the strength of maternal effects in animal populations. Ecol Lett 22:1620–1680

    PubMed  Google Scholar 

  • Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed effects models. Methods Ecol Evol 4:133–142

    Google Scholar 

  • Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18

    PubMed  Google Scholar 

  • Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, D.C.

    Google Scholar 

  • Pfennig DW (1990) The adaptive significance of an environmentally cued developmental switch in an anuran tadpole. Oecologia 85:101–107

    PubMed  Google Scholar 

  • Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to common evolutionary problem. Q Rev Biol 84:253–276

    PubMed  PubMed Central  Google Scholar 

  • Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467

    PubMed  Google Scholar 

  • Phillis CC, Moore JW, Buoro M, Hayes S, Garza JC, Pearse DE (2016) Shifting thresholds: rapid evolution of migratory life histories in steelhead/rainbow trout, Oncorhynchus mykiss. J Hered 107:51–60

    PubMed  Google Scholar 

  • Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427

    Google Scholar 

  • Ryan TJ, Plague GR (2004) Hatching asynchrony, survival, and the fitness of alternative adult morphs in Ambystoma talpoideum. Oecologia 140:46–51

    PubMed  Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Ecol 1:103–113

    Google Scholar 

  • Scott DE, Komoroski MJ, Croshaw DA, Dixon PM (2013) Terrestrial distribution of pond-breeding salamanders around an isolated wetland. Ecology 94:2537–2546

    PubMed  Google Scholar 

  • Searcy CA, Gray LN, Trenham PC, Shaffer HB (2014) Delayed life history effects, multilevel selection, and evolutionary trade-offs in the California tiger salamander. Ecology 95:68–77

    PubMed  Google Scholar 

  • Semlitsch RD (1987) Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying. Ecology 68:994–1002

    Google Scholar 

  • Semlitsch RD, Boone MD (2009) Aquatic mesocosms. In: Dodd CK (ed) Amphibian ecology and conservation: a handbook of techniques. Oxford University Press, Oxford, pp 87–104

    Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192

    Google Scholar 

  • Semlitsch RD, Harris RN, Wilbur HM (1990) Paedomorphosis in Ambystoma talpoideum: maintenance of population variation and alternative life-history pathways. Evolution 44:1604–1613

    PubMed  Google Scholar 

  • Smith TB, Skúlason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst 27:111–133

    Google Scholar 

  • Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283

    PubMed  Google Scholar 

  • Tachiki Y, Koizumi I (2016) Absolute and relative assessments of individual status in status-dependent strategies in stochastic environments. Am Nat 188:113–123

    PubMed  Google Scholar 

  • Tomkins JL, Brown GS (2004) Population density drives the local evolution of a threshold dimorphism. Nature 431:1099–1103

    CAS  PubMed  Google Scholar 

  • Tomkins JL, Hazel WN (2007) The status of the conditional evolutionary stable strategy. Trends Ecol Evol 22:522–528

    PubMed  Google Scholar 

  • Tomkins JL, Moczek AP (2009) Patterns of threshold evolution in polyphenic insects under different developmental models. Evolution 63:459–468

    PubMed  Google Scholar 

  • Tomkins JL, LeBas NR, Unrug J, Radwan J (2004) Testing the status dependent ESS model: population variation in fighter expression in the mite Sancassania berlesei. J Evol Biol 17:1377–1388

    CAS  PubMed  Google Scholar 

  • Tomkins JL, Hazel WN, Penrose MA, Radwan JW, LeBas NR (2011) Habitat complexity drives experimental evolution of a conditionally expressed secondary sexual trait. Curr Biol 21:569–573

    CAS  PubMed  Google Scholar 

  • Van Buskirk J, Cereghetti E, Hess JS (2017) Is bigger really better? Relative and absolute body size influence individual growth rate under competition. Ecol Evol 7:3745–3750

    PubMed  PubMed Central  Google Scholar 

  • Voss SR, Kump DK, Walker JA, Shaffer HB, Voss GJ (2012) Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders. Heredity 109:293–298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Warner DA, Shine R (2008) The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451:566–568

    CAS  PubMed  Google Scholar 

  • Warner RR, Fitch DL, Standish JD (1996) Social control of sex change in the shelf limpet, Crepidula norrisiarum: size-specific responses to local group composition. J Exp Mar Biol Ecol 204:155–167

    Google Scholar 

  • Watkins TB, McPeek MA (2006) Growth and predation risk in green frog tadpoles (Rana clamitans): a quantitative genetic analysis. Copeia 2006:478–488

    Google Scholar 

  • Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Wheeler DE (1991) The developmental basis of worker caste polymorphism in ants. Am Nat 138:1218–1238

    Google Scholar 

  • Whiteman HH (1994) Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221

    Google Scholar 

  • Whiteman HH (1997) Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51:2039–2044

    PubMed  Google Scholar 

  • Whiteman HH, Sheen JP, Johnson EB, VanDeusen A, Cargille R, Sacco TW (2003) Heterospecific prey and trophic polyphenism in larval tiger salamanders. 2003:56–67

    Google Scholar 

  • Whiteman HH, Krenz JD, Semlitsch RD (2006) Intermorph breeding and the potential for reproductive isolation in polymorphic mole salamanders (Ambystoma talpoideum). Behav Ecol Sociobiol 60:52–61

    Google Scholar 

  • Whiteman HH, Wissinger SA, Denoël M, Mecklin CJ, Gerlanc NM, Gutrich JJ (2012) Larval growth in polyphenic salamanders: making the best of a bad lot. Oecologia 168:109–118

    CAS  PubMed  Google Scholar 

  • Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302

    Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314

    CAS  PubMed  Google Scholar 

  • Wissinger SA, Whiteman HH, Denoël M, Mumford ML, Aubee CB (2010) Consumptive and nonconsumptive effects of cannibalism in fluctuating age-structured populations. Ecology 91:549–559

    PubMed  Google Scholar 

  • Ziemba RE, Collins JP (1999) Development of size structure in tiger salamanders: the role for intraspecific intereference. Oecologia 120:524–529

    PubMed  Google Scholar 

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Acknowledgements

We thank the many mentors who have patiently awaited this work, especially J.W. Gibbons. T. Ryan provided assistance in experimental monitoring. Feedback from T. Anderson, A. Lackey, M. Dugas, and members of the CWRU Ecology and Evolution reading group improved the presentation of the study. At various times throughout this long-gestating project, funding for MPM was provided by the Watershed Studies Institute (WSI), an MSU Graduate Innovation Assistantship, a GAANN Fellowship, the CWRU Department of Biology, as well as G. Kornblum and the Living Earth Collaborative. JHKP was funded by the Savannah River Ecology Laboratory (SREL), Florida International University, and Western Carolina University. HHW was funded by the SREL, WSI, the MSU Department of Biological Sciences, an MSU CISR award, and the NSF (DEB-1354787). Financial assistance was also provided by the Department of Energy Office of Environmental Management under award number DE-EM0004391. This report was prepared as an account of work sponsored by an agency of the United States Government. Neither the United States Government nor any agency thereof, nor any of their employees, makes any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product process, or service by trade name, trademark, manufacturer, or otherwise does not necessarily constitute or imply its endorsement, recommendation, or favoring by the United States Government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or any agency thereof.

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Authors and Affiliations

  1. Watershed Studies Institute and Department of Biological Sciences, Murray State University, Murray, KY, 42071, USA

    Michael P. Moore & Howard H. Whiteman

  2. Department of Biology, Case Western Reserve University, Cleveland, OH, 44106, USA

    Michael P. Moore

  3. Department of Biology, Western Carolina University, Cullowhee, NC, 28723, USA

    Joseph H. K. Pechmann

  4. Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, 29802, USA

    Joseph H. K. Pechmann & Howard H. Whiteman

  5. Living Earth Collaborative, Washington University, St. Louis, MO, 63105, USA

    Michael P. Moore

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  1. Michael P. Moore
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HHW and JHK designed the study and collected all data. MPM conducted all analyses and wrote the manuscript. All authors contributed to subsequent revisions

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Correspondence to Michael P. Moore.

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Communicated by Jean-François Le Galliard.

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Moore, M.P., Pechmann, J.H.K. & Whiteman, H.H. Relative size underlies alternative morph development in a salamander. Oecologia 193, 879–888 (2020). https://doi.org/10.1007/s00442-020-04723-8

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