Influences of facultative paedomorphosis on kin selection in a larval salamander, Ambystoma talpoideum

In: Behaviour
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  • a Department of Biological Sciences, Eastern Kentucky University, 521 Lancaster Avenue, Richmond, KY 40475, USA
  • b Department of Biology, Kentucky Wesleyan College, 3000 Frederica Street, Owensboro, KY 42301, USA
  • c Watershed Studies Institute and Department of Biological Sciences, Murray State University, Murray, KY 42071, USA

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Abstract

Kin selection in larval amphibians is hypothesized to increase survival to metamorphosis. While kin selection may benefit amphibians with obligate metamorphosis, increased survival within sibships may exert fitness costs on facultatively paedomorphic species, such as increased competition among kin. Consequently, it is unclear whether such species should engage in kin selection. We investigated kin selection in a facultatively paedomorphic salamander, Ambystoma talpoideum, using laboratory behavioural trials and microcosm experiments. Individuals were most aggressive towards familiar siblings, and full-sibship groups incurred more injuries than mixed-sibship groups; however, familiar siblings ultimately exhibited higher survival. Thus, while short-term responses appeared to reflect the hypothesized costs of kin recognition, long-term patterns of survival did not support this hypothesis. The inconsistencies between results suggest that short-term studies may not capture ontogenetic variation in kin selection, and that long-term studies are needed to better test the hypothesized effects of kin selection on survival and metamorphosis.

  • Abramoff, M.G., Magalhaes, P.J. & Ram, S. (2004). Image processing with ImageJ. — Biophotonics 11: 36-42.

  • Blaustein, A.R. (1983). Kin recognition mechanisms: phenotypic matching or recognition alleles? — Am. Nat. 121: 749-754.

  • Blaustein, A.R. & O’Hara, R.K. (1986). Kin recognition in tadpoles. — Sci. Am. 254: 108-116.

  • Blaustein, A.R. & Waldman, B. (1992). Kin recognition in anuran amphibians. — Anim. Behav. 44: 207-221.

  • Blaustein, A.R., Yoshikawa, T., Asoh, K. & Walls, S.C. (1993). Ontogenetic shifts in tadpole kin recognition: loss of signal and perception. — Anim. Behav. 46: 525-538.

    • Search Google Scholar
    • Export Citation
  • Bourke, A.F.G. (1997). Sociality and kin selection in insects. — In: Behavioural ecology: an evolutionary approach, 4th edn. (Krebs, J.R. & Davies, N.B., eds). Blackwell, Oxford, p. 203-227.

    • Search Google Scholar
    • Export Citation
  • Branch, L.C. & Altig, R. (1981). Nocturnal stratification of three species of Ambystoma larvae. — Copeia: 870-873.

  • Brodman, R. (2004). Intraguild predation on congeners affects size, aggression, and survival among Ambystoma larvae. — J. Herpetol. 38: 21-26.

    • Search Google Scholar
    • Export Citation
  • Brunkow, P.E. & Collins, J.P. (1998). Group size structure affects patterns of aggression in larval salamanders. — Behav. Ecol. 9: 508-514.

    • Search Google Scholar
    • Export Citation
  • Caley, M.J. & Boutin, S.A. (1987). Sibling and neighbor recognition in wild juvenile muskrats. — Anim. Behav. 35: 60-66.

  • Cockburn, A. (1998). Evolution of helping behavior in cooperatively breeding birds. — Annu. Rev. Ecol. Syst. 29: 141-177.

  • Crane, A., Mathis, A. & McGrane, C. (2012). Socially facilitated antipredator behavior by ringed salamander (Ambystoma annulatum). — Behav. Ecol. Sociobiol. 66: 811-817.

    • Search Google Scholar
    • Export Citation
  • Denoel, M., Joly, P. & Whiteman, H.H. (2005). Evolutionary ecology of facultative paedomorphosis in newts and salamanders. — Biol. Rev. 80: 663-671.

    • Search Google Scholar
    • Export Citation
  • Dugas, M.B., McCormack, L., Gadau, A. & Martin, R.A. (2016). Choosy cannibals preferentially consume siblings with relatively low fitness prospects. — Am. Nat. 188: 124-131.

    • Search Google Scholar
    • Export Citation
  • Emlen, S.T. (1997). Predicting family dynamics in social vertebrates. — In: Behavioural ecology: an evolutionary approach, 4th edn. (Krebs, J.R. & Davies, N.B., eds). Wiley-Blackwell, Oxford, p. 228-253.

    • Search Google Scholar
    • Export Citation
  • Frank, S.A. (1998). Foundations of social evolution. — Princeton University Press, Princeton, NJ.

  • Garza, S. & Waldman, B. (2015). Kin discrimination in polyphonic salamander larvae: trade-offs between inclusive fitness and pathogen transmission. — Behav. Ecol. Sociobiol. 69: 1473-1481.

    • Search Google Scholar
    • Export Citation
  • Griffiths, S.W. & Armstrong, J.D. (2002). Kin-biased territory overlap and food sharing among Atlantic salmon. — J. Anim. Ecol. 71: 480-486.

    • Search Google Scholar
    • Export Citation
  • Hamilton, W.D. (1964). The genetic evolution of social behavior. I-II. — J. Theor. Biol. 7: 1-52.

  • Harris, R.N., Vess, T.J., Hammond, J.I. & Lindermuth, C.J. (2003). Context-dependent kin discrimination in larval four-toed salamanders Hemidactylium scutatum (Caudata: Plethodontidae). — Herpetologica 59: 164-177.

    • Search Google Scholar
    • Export Citation
  • Hatchwell, B.J. (2010). Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. — J. Ethol. 116: 203-216.

    • Search Google Scholar
    • Export Citation
  • Hepper, P.G. & Cleland, J. (1999). Developmental aspects of kin recognition. — Genetica 104: 199-205.

  • Hokit, G.D., Walls, S.C. & Blaustein, A.R. (1996). Context-dependent kin discrimination in larvae of the marbled salamander, Ambystoma opacum. — Anim. Behav. 52: 17-31.

    • Search Google Scholar
    • Export Citation
  • Horne, M.T. & Dunson, W.A. (1995). Effects of low pH, metals, and water hardness on larval amphibians. — Arch. Environ. Con. Tox. 29: 500-505.

    • Search Google Scholar
    • Export Citation
  • Ireland, P.H. (1989). Larval survivorship in two populations of Ambystoma maculatum. — J. Herpetol. 23: 209-215.

  • Kaplan, R.H. (1980). The implications of ovum size variability for offspring fitness and clutch size with several populations of salamanders (Ambystoma). — Evolution 34: 51-64.

    • Search Google Scholar
    • Export Citation
  • Kareem, A.M. & Barnard, C.J. (1982). The importance of kinship and familiarity in social interactions between mice. — Anim. Behav. 30: 594-601.

    • Search Google Scholar
    • Export Citation
  • Kusano, T., Kusano, H. & Miyashita, K. (1985). Size-related cannibalism among larval Hynobious nebulosus. — Copeia: 472-476.

  • Liebgold, E.B. & Dibble, C.J. (2011). Better the devil you know: familiarity affects foraging activity of red-backed salamanders, Plethodon cinereus. — Anim. Behav. 82: 1059-1066.

    • Search Google Scholar
    • Export Citation
  • Maret, T.J. & Collins, J.P. (1994). Individual responses to population size structure: the role of size variation in controlling expression of a trophic polyphenism. — Oecologia 100: 279-285.

    • Search Google Scholar
    • Export Citation
  • Markman, S., Hill, N., Todrank, J., Heth, G. & Blaustein, L. (2009). Differential aggressiveness between fire salamander (Salamandra infraimmaculata) larvae covaries with their genetic similarity. — Behav. Ecol. Sociobiol. 8: 1149-1155.

    • Search Google Scholar
    • Export Citation
  • Mathis, A., Jaeger, R.G., Keen, W.H., Ducey, P.K., Walls, S.C. & Buchanan, B.W. (1995). Aggression and territoriality by salamanders and a comparison with the territorial behavior of frogs. — In: Amphibian biology, Vol. 2 (Heatwole, H. & Sullivan, B.K., eds). Surrey Beatty & Sons, Chipping Norton, NSW, p. 633-676.

    • Search Google Scholar
    • Export Citation
  • Moore, M.P., Landberg, T. & Whiteman, H.H. (2015). Maternal investment mediates offspring life history variation with context-dependent fitness consequences. — Ecology 96: 2499-2509.

    • Search Google Scholar
    • Export Citation
  • Mott, C.L., Albert, S.E., Steffen, M.A. & Uzzardo, J.M. (2010). Assessment of digital image analyses for use in wildlife research. — Wild. Biol. 16: 93-100.

    • Search Google Scholar
    • Export Citation
  • Mott, C.L. & Maret, T.J. (2010). Species-specific patterns of agonistic behavior among larvae of three syntopic species of ambystomatid salamanders. — Copeia: 9-17.

    • Search Google Scholar
    • Export Citation
  • Oldham, R.S. (1966). Spring movements in the American toad, Bufo americanus. — Can. J. Zool. 44: 63-100.

  • Pakkasmaa, S. & Laurila, A. (2004). Are the effects of kinship modified by environmental conditions in Rana temporaria tadpoles? — Ann. Zool. Fenn. 41: 413-420.

    • Search Google Scholar
    • Export Citation
  • Petranka, J.W. (1984). Incubation, larval growth, and embryonic and larval survivorship of smallmouth salamanders (Ambystoma texanum) in streams. — Copeia: 862-868.

    • Search Google Scholar
    • Export Citation
  • Petranka, J.W. (1998). Salamanders of the United States and Canada. — Smithsonian Institute Press, Washington, DC.

  • Pfennig, D.W. (1999). Cannibalistic tadpoles that pose the greatest threat to kin are most likely to discriminate kin. — Proc. Roy. Soc. Lond. B: Biol. Sci. 266: 57-61.

    • Search Google Scholar
    • Export Citation
  • Pfennig, D.W., Loeb, M.L.G. & Collins, J.P. (1991). Pathogens as a factor limiting the spread of cannibalism in tiger salamanders. — Oecologia 88: 161-166.

    • Search Google Scholar
    • Export Citation
  • Pfennig, D.W., Reeve, H.K. & Sherman, P.W. (1993). Kin recognition and cannibalism in spadefoot toad tadpoles. — Anim. Behav. 46: 87-94.

    • Search Google Scholar
    • Export Citation
  • Pfennig, D.W., Sherman, P.W. & Collins, J.P. (1994). Kin recognition and cannibalism in polyphenic salamanders. — Behav. Ecol. 5: 225-232.

    • Search Google Scholar
    • Export Citation
  • Pfennig, D.W., Collins, J.P. & Ziemba, R.E. (1999). A test of alternative hypotheses for kin recognition in cannibalistic tiger salamanders. — Behav. Ecol. 10: 436-443.

    • Search Google Scholar
    • Export Citation
  • Platt, T.J. & Bever, J.D. (2009). Kin competition and the evolution of cooperation. — Trends Ecol. Evol. 24: 370-377.

  • Rudolf, V.H.W. & Antonovics, J. (2007). Disease transmission by cannibalism: rare event or common occurrence? — Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 1205-1210.

    • Search Google Scholar
    • Export Citation
  • Scott, D.E. (1994). The effect of larval density on adult demographic traits in Ambystoma opacum. — Ecology 75: 1383-1396.

  • Scott, D.E., Komoroski, M.J., Croshaw, D.A. & Dixon, P.M. (2013). Terrestrial distribution of pond-breeding salamanders around an isolated wetland. — Ecology 94: 2537-2546.

    • Search Google Scholar
    • Export Citation
  • Semlitsch, R.D. & Reichling, S.B. (1989). Density-dependent injury in larval salamanders. — Oecologia 81: 100-103.

  • Van Buskirk, J. & Smith, D.C. (1991). Density-dependent population regulation in a salamander. — Ecology 72: 1747-1756.

  • Waldman, B. (1984). Kin recognition and sibling association among wood frog (Rana sylvatica) tadpoles. — Behav. Ecol. Sociobiol. 14: 171-180.

    • Search Google Scholar
    • Export Citation
  • Waldman, B. (1988). The ecology of kin recognition. — Annu. Rev. Ecol. Syst. 19: 543-571.

  • Walls, S.C. (1991). Ontogenetic shifts in the recognition of siblings and neighbors by juvenile salamanders. — Anim. Behav. 42: 423-434.

    • Search Google Scholar
    • Export Citation
  • Walls, S.C. & Blaustein, A.R. (1994). Does kinship influence density dependence in a larval salamander? — Oikos 71: 459-468.

  • Walls, S.C. & Blaustein, A.R. (1995). Larval marbled salamanders, Ambystoma opacum, eat their kin. — Anim. Behav. 50: 537-545.

  • Walls, S.C. & Jaeger, R.G. (1987). Aggression and exploitation as mechanisms of competition in larval salamanders. — Can. J. Zool. 65: 2938-2944.

    • Search Google Scholar
    • Export Citation
  • Walls, S.C. & Roudebush, R.E. (1991). Reduced aggression towards siblings as evidence of kin recognition in cannibalistic salamanders. — Am. Nat. 138: 1027-1038.

    • Search Google Scholar
    • Export Citation
  • Walls, S.C. & Semlitsch, R.D. (1991). Visual and movement displays function as agonistic behavior in larval salamanders. — Copeia 1991: 936-942.

    • Search Google Scholar
    • Export Citation
  • Ward, A.J.W. & Hart, P.J.B. (2003). The effects of kin and familiarity on interactions between fish. — Fish Fish. 4: 348-358.

  • West Eberhard, M.J. (1975). The evolution of social behavior by kin selection. — Q. Rev. Biol. 50: 1-33.

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

  • Whiteman, H.H. (1994). Evolution of facultative paedomorphosis in salamanders. — Q. Rev. Biol. 69: 205-221.

  • Whiteman, H.H., Wissinger, S.A. & Brown, W.S. (1996). Growth and foraging consequences of facultative paedomorphosis in the tiger salamander, Ambystoma tigrinum nebulosum. — Evol. Ecol. 10: 433-446.

    • Search Google Scholar
    • Export Citation
  • Whiteman, H.H., Krenz, J.D. & Semlitsch, R.D. (2006). Intermorph breeding and the potential for reproductive isolation in polymorphic mole salamanders (Ambystoma talpoideum). — Behav. Ecol. Sociobiol. 60: 52-61.

    • Search Google Scholar
    • Export Citation
  • Wilbur, H.M. & Collins, J.P. (1973). Ecological aspects of amphibian metamorphosis. — Science 182: 1305-1314.

  • Wildy, E.L. & Blaustein, A.R. (2001). Learned recognition of intraspecific predators in larval long-toed salamanders Ambystoma macrodactylum. — J. Ethol. 107: 479-493.

    • Search Google Scholar
    • Export Citation
  • Wildy, E.L., Chivers, D.P., Kiesecker, J.M. & Blaustein, A.R. (2001). The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum. — Oecologia 128: 202-209.

    • Search Google Scholar
    • Export Citation
  • Winn, B.E. & Vestal, B.M. (1986). Kin recognition and choice of males by wild female house mice (Mus musculus). — J. Comp. Psychol. 100: 72-75.

    • Search Google Scholar
    • Export Citation
  • Ydenberg, R.C., Giraldeau, L.A. & Falls, J.B. (1988). Neighbors, strangers, and the asymmetric war of attrition. — Anim. Behav. 36: 343-347.

    • Search Google Scholar
    • Export Citation
  • Ziemba, R.E. & Collins, J.P. (1999). Development of size structure in tiger salamanders: the role of intraspecific interference. — Oecologia 120: 524-529.

    • Search Google Scholar
    • Export Citation

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