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The relationship between genetic variability and growth rate among populations of the pocket gopher, Thomomys bottae

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Abstract

Perhaps the oldest unresolved debate inconservation genetics is whether geneticvariability matters – in other words, whetherrelatively low average genetic variationcontributes to deficits in individual andpopulation level vigor and fitness. Using astatistically powerful paired sampling designin which each of three pairs of populationsconsisted of one high genetic variability andone low genetic variability population from aparticular subspecies of the pocket gopher,Thomomys bottae, we tested the hypothesisthat individuals from populations with lowergenetic variability have lower growth rates (acommonly used surrogate for fitness) than thosefrom populations with higher variability. Wemeasured genetic variability using averageallozyme heterozygosity and two measures of DNAfingerprint band sharing (Jeffreys 33.15 andMS1 probes). The population rankings of thelevels of genetic variability among the threemeasures were concordant. The least squaresmean growth rate (controlling for sex,subspecies and initial mass) of gophers fromlow variability populations (0.41 ± 0.06g/day, n = 48) was less than half that ofgophers from high variability populations (1.04± 0.07 g/day, n = 45). This result lendscredence to the premise that differences inpopulation level genetic variability havesignificant fitness consequences andunderscores the importance of maintaininggenetic variability in managed populations.

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References

  • Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Conservation Biology: The Science of Scarcity and Diversity (ed. Soulé ME), pp. 57–86. Sinauer Associates, Inc., Sunderland, Massachusetts.

    Google Scholar 

  • Ballou JD (1997) Effects of ancestral inbreeding on genetic load in mammalian populations. Journal of Heredity, 88, 169–178.

    Google Scholar 

  • Bijlsma R, Bundgaard J, Van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol., 12, 1125–1137.

    Google Scholar 

  • Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila. J. Evol. Biol., 13, 502–514.

    Google Scholar 

  • Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science, 184, 908–909.

    Google Scholar 

  • Britten HB (1996) Meta-analyses of the association between multilocus heterozygosity and fitness. Evolution, 50, 2158–2164.

    Google Scholar 

  • Burnham KP, Anderson DR (1998) Model Selection and Inference: A Practical Information-Theoretic Approach. Springer, New York.

    Google Scholar 

  • Caro RM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science, 263, 485–486.

    Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J. Anim. Ecol., 63, 215–244.

    Google Scholar 

  • Coltman DW, Bowen WD, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B Biol. Sci., 265, 803–809.

    Google Scholar 

  • Cothran EG, Chesser RK, Smith MH, Johns PE (1983) Influences of genetic variability and maternal factors on fetal growth in whitetailed deer. Evolution, 37, 282–291.

    Google Scholar 

  • Coulson TN, Pemberton JM, Albon SD, Beaumont M, Marshall TC, Slate J, Guinness FE, Clutton-Brock TH (1998) Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B Biol. Sci., 265, 489–495.

    Google Scholar 

  • Daly JC, Patton JL (1990) Dispersal, gene flow, and allelic diversity between local populations of Thomomys bottae pocket gophers in the coastal ranges of California. Evolution, 44, 1283–1294.

    Google Scholar 

  • Dawson WR, Lignon JD, Murphy JR, Myers JP, Simberloff D, Verner J (1987) Report of the scientific advisory panel on the spotted owl. Condor, 89, 205–229.

    Google Scholar 

  • Fitzsimmons NN, Buskirk SW, Smith MH (1995) Population history, genetic variability, and horn growth in bighorn sheep. Conserv. Biol., 9, 314–323.

    Google Scholar 

  • Foster GG, Hodgson AN, Balarin M (1999) Effect of diet on growth rate and reproductive fitness of Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Mar. Biol. (Berlin), 134, 307–315.

    Google Scholar 

  • Frankham R (1995) Inbreeding and extinction: A threshold effect. Conserv. Biol., 9, 792–799.

    Google Scholar 

  • Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: Effects of purging. Conservation Genetics, 2, 279–285.

    Google Scholar 

  • Haikola S, Fortelius W, O'Hara RB, Kuussaari M, Wahlberg N, Saccheri IJ, Singer MC, Hanski I (2001) Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations. Conservation Genetics, 2, 325–335.

    Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu. Rev. Ecol. Syst., 31, 139–162.

    Google Scholar 

  • Hildner KK (2000) The Relationship Between Genetic Variability and Physiological Fitness Among Populations of the Pocket Gopher, Thomomys bottae, and its Implications for Conservation. PhD Dissertation, University of California Santa Cruz, Santa Cruz, CA.

    Google Scholar 

  • Hoelzel AR, Halley J, O'Brien SJ, Campagna C, Arnbom T, Boeuf BL, Ralls K, Dover GA (1993) Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. J. Heredity, 84, 443–449.

    Google Scholar 

  • Howard WE, Childs HE (1959) Ecology of pocket gophers with emphasis on Thomomys bottae mewa. Hilgardia, 29, 277–358.

    Google Scholar 

  • Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable “minisatellite” regions in human DNA. Nature, 314, 67–73.

    Google Scholar 

  • Jeffreys AJ, Nicola JR, Wilson V, Wong Z (1988) Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature, 332, 278–281.

    Google Scholar 

  • Jimenez JA, Hughes KA, Alaks G, Graham L, Lacy RC (1994) An experimental study of inbreeding depression in a natural habitat. Science, 266, 271–273.

    Google Scholar 

  • Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution, 52, 240–250.

    Google Scholar 

  • Keller LF, Waller DM(2002) Inbreeding effects in wild populations. Trends Ecol. Evol., 17, 230–241.

    Google Scholar 

  • Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J. Mammal., 78, 320–335.

    Google Scholar 

  • Lacy RC, Ballou JD (1998) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution, 52, 900–909.

    Google Scholar 

  • Lampert W, Trubetskova T (1996) Juvenile growth rate as a measure of fitness in Daphnia. Funct. Ecol., 10, 631–635.

    Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science, 241, 1455–1460.

    Google Scholar 

  • Lynch M (1990) The similarity index and DNA fingerprinting. Mol. Biol. Evol., 7, 478–484.

    Google Scholar 

  • Miller MA (1946) Reproductive rates and cycles in the pocket gopher. J. Mammal., 27, 335–358.

    Google Scholar 

  • Mills LS, Smouse PE (1994) The demographic consequences of inbreeding in small remnant populations. Amer. Natur., 144, 412–431.

    Google Scholar 

  • Mitton JB (1997) Selection in Natural Populations. Oxford University Press, Oxford.

    Google Scholar 

  • Nieminen M, Singer MC, Fortelius W, Schops K, Hanski I (2001) Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Amer. Natur., 157, 237–244.

    Google Scholar 

  • Ouborg NJ, Groenendael JMV (1996) Demography, genetics, or statistics: comments on a paper by Heschel and Paige. Conserv. Biol., 10, 1290–1291.

    Google Scholar 

  • Patton JL, Yang SY (1977) Genetic variation in Thomomys bottae pocket gophers: macrogeographic patterns. Evolution, 31, 697–720.

    Google Scholar 

  • Patton JL, Brylski PV (1987) Pocket gophers in alfalfa fields: causes and consequences of habitat-related body size variation. Amer. Natur., 130, 493–506.

    Google Scholar 

  • Patton JL, Smith MF (1990) The evolutionary dynamics of the pocket gopher Thomomys bottae, with emphasis on California populations. Univ. Cal. Press Publ. Zool., 123, 1–161.

    Google Scholar 

  • Patton JL, Selander RK, Smith MH (1972) Genic variation in hybridizing populations of gophers (genus Thomomys). Syst. Zool., 21, 263–270.

    Google Scholar 

  • Pimm SL, Jones HL, Diamond J (1988) On the risk of extinction. Amer. Natur., 132, 757–785.

    Google Scholar 

  • Pimm SL, Gittlemann JL, McCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol. Evol., 4, 176–178.

    Google Scholar 

  • Presley ML, McElroy TC, Diehl WJ (1996) Soil moisture and temperature interact to affect growth, survivorship, fecundity, and fitness in the earthworm Eisenia fetida. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 114, 319–326.

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, U.K.; New York.

    Google Scholar 

  • Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol., 2, 185–193.

    Google Scholar 

  • Reed DH, Bryant EH (2000) Experimental test of minimum viable population size. Anim. Conserv., 3, 7–14.

    Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Pia V, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491–494.

    Google Scholar 

  • Sanjayan MA (1997) Genetic Variation, Physiology, and Survival in a Natural Population of Pocket Gophers. PhD Dissertation, University of California Santa Cruz, Santa Cruz, CA.

    Google Scholar 

  • Sanjayan MA, Crooks K, Zegers G, Foran D (1996) Genetic variation and the immune response in natural populations of pocket gophers. Conserv. Biol., 10, 1519–1527.

    Google Scholar 

  • Schwartz OA, Bleich VC, Holl SA (1986) Genetics and conservation of mountain sheep Ovis canadensis nelsoni. Biol. Conserv., 37, 179–190.

    Google Scholar 

  • Selander RK, Smith MH, Yang S, Johnson WE, Gentry JB (1971) Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Univ. of Texas Publ., 7103, 49–90.

    Google Scholar 

  • Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proc. R. Soc. Lond. B Biol. Sci., 249, 163–171.

    Google Scholar 

  • Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc. R. Soc. Lond. B Biol. Sci., 267, 1657–1662.

    Google Scholar 

  • Soulé ME (1987) Where do we go from here? In: Viable Populations for Conservation (ed. Soulé ME), pp. 175–184. Cambridge University Press, Cambridge.

    Google Scholar 

  • Soulé ME, Mills LS (1998) Population genetics–No need to isolate genetics. Science, 282, 1658–1659.

    Google Scholar 

  • Zar JH (1984) Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, NJ.

    Google Scholar 

  • Zimmerman (1993) SIM ver. 1.01. University of California Regents.

  • Zouros E (1987) On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine mollusks. Isozymes Curr. Topics Biol. Med. Res., 15, 255–270.

    Google Scholar 

  • Zouros E, Foltz DW (1987) The use of allelic isozyme variation for the study of heterosis. Isozymes Curr. Topics Biol. Med. Res., 13, 1–59.

    Google Scholar 

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, CA, 95064, USA

    K. Kelly Hildner

  2. P.O. Box 2010, Hotchkiss, CO, 81419, USA

    Michael E. Soulé

  3. Seoul National University School of Agricultural Biotechnology and College of Veterinary Medicine, Seoul, 151-742, Korea

    Mi-Sook Min

  4. Forensic Biology Program, School of Criminal Justice and Department of Zoology, 560 Baker Hall, Michigan State University, East Lansing, MI, 48824, USA

    David R. Foran

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  1. K. Kelly Hildner
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  2. Michael E. Soulé
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Correspondence to K. Kelly Hildner.

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Hildner, K.K., Soulé, M.E., Min, MS. et al. The relationship between genetic variability and growth rate among populations of the pocket gopher, Thomomys bottae . Conservation Genetics 4, 233–240 (2003). https://doi.org/10.1023/A:1023319608750

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