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Natal philopatry varies with larval condition in salamanders

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Abstract

An individual’s physiological condition early in ontogeny often regulates natal dispersal and philopatry decisions; however, increased condition promotes dispersal in some organisms and philopatry in others. These disparate findings likely arise from interactions among an individual’s early life stage physiological condition, its likelihood of surviving a dispersal event (i.e., dispersal capacity), and its motivation to leave its natal site (i.e., dispersal propensity). Due to the broad importance of reproductive site selection to population structure and dynamics, studies disentangling these various phenotype-dependent effects are critical. We evaluated the relationships between two aspects of larval physiological condition and natal philopatry in Arizona tiger salamanders (Ambystoma tigrinum nebulosum) in an isolated pond system. In this population, geographic distance between ponds is small, adult survivorship is very high, and thus the likelihood of a successful breeding event should mediate reproductive site selection as opposed to the likelihood of surviving the dispersal event. We found that natal philopatry increased with an estimate of long-term body condition in males, but there was no relationship in females. However, natal philopatry decreased with an estimate of short-term body condition. We also found that an individual’s natal pond had effects on philopatry that influenced both sexes and were independent of the pond’s direct effects on body condition. Together, these findings strongly support the importance of an individual’s early developmental experience in the natal environment to its reproductive behaviors across its lifespan, and further highlight the value of considering how phenotype-dependent dispersal mechanisms may vary between the sexes.

Significance statement

Previous research has not discerned a generalizable relationship between larval physiological condition and natal philopatry, likely because of the complex interaction between an individual’s ability (dispersal capacity) and its motivation (dispersal propensity) to reproduce in its natal habitat. Using a salamander population with small inter-pond distances and high adult survival, we isolated the effects of two aspects of physiological condition on dispersal propensity. We found that increased long-term larval physiological condition was associated with natal philopatry in male, but not female, tiger salamanders, as well as differences in philopatry based on natal pond. In contrast, short-term larval physiological condition was negatively associated with philopatry. Our findings suggest an important, long-lasting role of the natal environment on reproductive site selection, and further implicate that the conditions experienced in early development can strongly affect reproductive behaviors across the life cycle.

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References

  • Anholt BR (1990) Size-biased dispersal prior to breeding in a damselfly. Oecologia 83:385–387

    Article  Google Scholar 

  • Auillon SM, Duckworth RA (2015) Kin aggression and resource availability influence phenotype-dependent dispersal in a passerine bird. Behav Ecol Sociobiol 69:625–633

    Article  Google Scholar 

  • Baines CB, McCauley SJ, Rowe L (2015) Dispersal depends on body condition and predation risk in the semi-aquatic insect Notonecta undulata. Ecol Evol 5:2307–2316

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbraud C, Johnson AR, Bertault G (2003) Phenotypic correlates of post-fledging dispersal in a population of greater flamingos: the importance of body condition. J Anim Ecol 72:246–257

    Article  Google Scholar 

  • Benard MF, McCauley SJ (2008) Integrating across life-history stages: consequences of natal habitat effects on dispersal. Am Nat 171:553–567

    Article  PubMed  Google Scholar 

  • Bohanak AJ, Whiteman HH (1999) Dispersal of the fairy shrimp Branchinecta coloradensis (Anostraca): effects of hydroperiod and salamanders. Limnol Oceanogr 44:487–493

    Article  Google Scholar 

  • Bonte D, de la Peña E (2009) Evolution of body condition-dependent dispersal in metapopulations. J Evol Biol 22:1242–1251

    Article  CAS  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behavior to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Byers J, Dunn S (2012) Bateman in nature: predation on offspring reduces the potential for sexual selection. Science 338:802–804

    Article  CAS  PubMed  Google Scholar 

  • Calsbeek R (2009) Sex-specific adult dispersal and its selective consequences in the brown anole, Anolis sagrei. J Anim Ecol 78:617–624

    Article  PubMed  Google Scholar 

  • Champan T, Arnqvis G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  • Chaput-Bardy A, Grégoire A, Baguette M, Pagano A, Secondi J (2010) Condition and phenotype-dependent dispersal in a damselfly, Calopteryx splendens. PLoS ONE 5, e10694

    Article  PubMed  PubMed Central  Google Scholar 

  • Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • Cornwallis CK, Uller T (2010) Towards an evolutionary ecology of sexual traits. Trends Ecol Evol 25:145–152

    Article  PubMed  Google Scholar 

  • Cote J, Clobert J (2010) Risky dispersal: avoiding kin competition despite uncertainty. Ecology 91:1485–1493

    Article  CAS  PubMed  Google Scholar 

  • Debeffe L, Morellet N, Cargnelutti B, Lourtet B, Bon R, Gaillard JM, Hewison AJM (2012) Condition-dependent natal dispersal in a large herbivore: heavier animals show a greater propensity to disperse and travel further. J Anim Ecol 81:327–337

    Article  Google Scholar 

  • Denoël M, Hervant F, Schabetsberger R, Joly P (2002) Short- and long-term advantages of an alternative ontogenetic pathway. Biol J Linn Soc 77:105–112

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Earl JE, Whiteman HH (2015) Are commonly used fitness predictors accurate? A meta-analysis of amphibian size and age at metamorphosis. Copeia 103:297–309

    Article  Google Scholar 

  • Feder ME, Burggren WW (1992) Environmental physiology of the amphibians. University of Chicago Press, Chicago

    Google Scholar 

  • Forero MG, Donázar JA, Hiraldo F (2002) Causes and fitness consequences of natal dispersal in a population of black kites. Ecology 83:858–872

    Article  Google Scholar 

  • Howard RD (1978) The influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecology 59:789–798

    Article  Google Scholar 

  • Howard RD (1983) Sexual selection and variation in reproductive success in a long-lived organism. Am Nat 122:301–325

    Article  Google Scholar 

  • Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

    Article  Google Scholar 

  • Jones OR, Scheuerlein A, Salguero-Gómez R et al (2014) Diversity of ageing across the tree of life. Nature 505:169–173

    Article  CAS  PubMed  Google Scholar 

  • Kiesecker JM, Skelly DK (2000) Choice of oviposition site by gray treefrogs: the role of potential parasitic infection. Ecology 81:2939–2943

    Article  Google Scholar 

  • McCauley SJ (2010) Body size and social dominance influence breeding dispersal in male Pachydiplax longipennis (Odonata). Ecol Entomol 35:377–385

    Article  Google Scholar 

  • McPeek MA, Holt RD (1992) The evolution of dispersal in spatially and temporally varying environments. Am Nat 140:1010–1027

  • Meylan S, Belliure J, Clobert J, de Fraipont M (2002) Stress and body condition as prenatal and postnatal determinants of dispersal in the common lizard. Horm Behav 42:319–326

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421–431

  • Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661

    Article  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/

  • Resetarits WJ Jr (1996) Oviposition site choice and life history evolution. Am Zool 36:205–215

    Article  Google Scholar 

  • Resetarits WJ Jr, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220–228

    Article  Google Scholar 

  • Rose CS (2005) Integrating ecology and developmental biology to explain the timing of frog metamorphosis. Trends Ecol Evol 20:129–135

    Article  PubMed  Google Scholar 

  • Saastamoinen M, van der Sterren D, Vastenhout N, Zwaan BJ, Brakefield PM (2010) Predictive adaptive responses: condition-dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. Am Nat 176:686–698

    Article  PubMed  Google Scholar 

  • Sadeh A, Mangel M, Blaustein L (2009) Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics. Ecol Lett 12:1158–1164

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Scott DE, Casey ED, Donovan MF, Lynch TK (2007) Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival. Oecologia 153:521–532

    Article  PubMed  Google Scholar 

  • Sinervo B, Calsbeek R, Comendant T, Both C, Adamopoulou C, Clobert J (2006) Genetic and maternal determinants of effective dispersal: the effect of sire genotype and size at birth in side-blotched lizards. Am Nat 168:88–99

    Article  PubMed  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128

  • Szulkin M, Sheldon BC (2008) Dispersal as a means of inbreeding avoidance in a wild bird population. Proc R Soc Lond B 275:703–711

    Article  Google Scholar 

  • Tarwater CE, Beissinger SR (2012) Dispersal polymorphisms from natal phenotype-environment interactions have carry-over effects on lifetime reproductive success of a tropic parrot. Ecol Lett 15:1218–1229

    Article  PubMed  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Whiteman HH, Wissinger SA (2005) Amphibian population cycles and long-term data sets. In: Lanoo ML (ed) Amphibian declines: conservation status of U.S. species. University of California Press, Berkeley, pp 177–184

    Chapter  Google Scholar 

  • Whiteman HH, Howard RD, Whitten KA (1995a) Effects of pH on embryo tolerance and adult behavior in the tiger salamander, Ambystoma tigrinum tigrinum. Can J Zool 73:1529–1537

    Article  Google Scholar 

  • Whiteman HH, Wissinger SA, Bohonak AJ (1995b) Seasonal movement patterns in a high-elevation population of the tiger salamander, Ambystoma tigrinum nebulosum. Can J Zool 72:1780–1787

    Article  Google Scholar 

  • Whiteman HH, Gutrich JJ, Moorman RS (1999) Courtship behavior in a polymorphic population of tiger salamander, Ambystoma tigrinum nebulosum. J Herpetol 33:348–351

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Whiteman HH, Doyle JM, Aubee C, Brown R, Thomason S, Schoborg T (2016) A PIT tagging technique for ambystomatid salamanders. Herpetol Rev 47:32–34

    Google Scholar 

  • Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wissinger SA, Whiteman HH (1992) Fluctuation in a Rocky Mountain population of salamanders: anthropogenic acidification or natural variation? J Herpetol 26:377–391

    Article  Google Scholar 

  • Wissinger SA, Bohonak AJ, Whiteman HH, Brown WS (1999) Subalpine wetlands in Colorado: habitat permanence, salamander predation, and invertebrate communities. In: Batzer DP, Wissinger SA (eds) Invertebrates in freshwater wetlands of North America: ecology and management. Wiley, New York, pp 757–790

    Google Scholar 

  • Wissinger SA, Brown WS, Jannot JE (2003) Caddisfly life histories along permanence gradients in high-altitude wetlands in Colorado (U.S.A.). Freshw Biol 48:255–270

    Article  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

    Article  PubMed  Google Scholar 

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Acknowledgments

This long-term research could not have been completed without the support and assistance of numerous colleagues, research assistants, and funding agencies. We particularly thank R.D. Howard and S.A. Wissinger for much needed advice, wisdom, and insight, and S.A. Wissinger, M. Denoel, N. Gerlanc, A. Lackey, W. Brown, A. Benson, J. Boynton, E. Olson, J. Doyle, J. Earl, T. Anderson, M. Geile, A. Bohonak, S. Horn, J. Gutrich, and C. Aubee and numerous other undergraduate RAs provided field and intellectual assistance. I. Billick, J. Reithel, B. Barr, S. Donovan, S. Lohr, T. Allison, and L. Swift have provided much needed aid and assistance at the RMBL, and W. Gibbons, R. Semlitsch, D. White, and G. Kipphut patiently supported this work. M. Dugas, R. Martin, T. Anderson, A. Lackey, B. Tumolo, S. Strickler, H. Rollins, D. Pfennig, members of the Whiteman Lab, and several anonymous reviewers all provided invaluable feedback that substantially improved the quality of the manuscript. P. Bergeron and S. Crosby provided much needed distractions. MPM was supported by the Watershed Studies Institute, the Murray State University Graduate Innovation Assistantship, and the Department of Biology at Case Western Reserve University. HHW was funded by a Purdue David Ross Summer Fellowship, a Purdue Research Foundation Fellowship, the American Museum of Natural History (Theodore Roosevelt Fund), Sigma Xi (Grant in Aid), the Rocky Mountain Biological Laboratory (Lee RG Snyder Memorial Fund), the American Society of Ichthyologists and Herpetologists (Helen Gaige Fund), the Animal Behavior Society (ABS Research Grant), the Colorado Division of Wildlife, the American Philosophical Society, the Murray State University Center for Institutional Studies and Research (CISR), a CISR Presidential Research Fellowship, the Watershed Studies Institute, and especially the National Science Foundation (DEB-9122981, DEB-0109436, and DEB-1354787 to HHW; EPI-0132295 to G. Kipphut; and UBM-0531865 and UBM-1028125 to R. Fister).

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  1. Michael P. Moore

    Present address: Department of Biology, Case Western Reserve University, 2080 Adelbert Road, Cleveland, OH, 44106, USA

Authors and Affiliations

  1. Watershed Studies Institute, Murray State University, Murray, KY, 42071, USA

    Michael P. Moore & Howard H. Whiteman

  2. Rocky Mountain Biological Laboratory, P.O. Box 519, Crested Butte, CO, 81224, USA

    Michael P. Moore & Howard H. Whiteman

  3. Department of Biological Sciences, Murray State University, Murray, KY, 42071, USA

    Howard H. Whiteman

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All protocols were approved by the Murray State and RMBL Institutional Animal Care and Use Committees, and all animals were captured under Colorado Parks and Wildlife Permit HP-0339.

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Communicated by D. W. Pfennig

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Moore, M.P., Whiteman, H.H. Natal philopatry varies with larval condition in salamanders. Behav Ecol Sociobiol 70, 1247–1255 (2016). https://doi.org/10.1007/s00265-016-2133-z

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