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Adult survival and microsatellite diversity in possums: effects of major histocompatibility complex-linked microsatellite diversity but not multilocus inbreeding estimators

Abstract

Adult survival is perhaps the fitness parameter most important to population growth in long-lived species. Intrinsic and extrinsic covariates of survival are therefore likely to be important drivers of population dynamics. We used long-term mark-recapture data to identify genetic, individual and environmental covariates of local survival in a natural population of mountain brushtail possums (Trichosurus cunninghami). Rainfall and intra-individual diversity at microsatellite DNA markers were associated with increased local survival of adults and juveniles. We contrasted the performance of several microsatellite heterozygosity measures, including internal relatedness (IR), homozygosity by loci (HL) and the mean multilocus estimate of the squared difference in microsatellite allele sizes within an individual (mean d 2). However, the strongest effect on survival was not associated with multilocus microsatellite diversity (which would indicate a genome-wide inbreeding effect), but a subset of two loci. This included a major histocompatibility complex (MHC)-linked marker and a putatively neutral microsatellite locus. For both loci, diversity measures incorporating allele size information had stronger associations with survival than measures based on heterozygosity, whether or not allele frequency information was included (such as IR). Increased survival was apparent among heterozygotes at the MHC-linked locus, but the benefits of heterozygosity to survival were reduced in heterozygotes with larger differences in allele size. The effect of heterozygosity on fitness-related traits was supported by data on endoparasites in a subset of the individuals studied in this population. There was no apparent density dependence in survival, nor an effect of sex, age or immigrant status. Our findings suggest that in the apparent absence of inbreeding, variation at specific loci can generate strong associations between fitness and diversity at linked markers.

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Notes

  1. 1.

    We also used generalised linear models to test for potential effects of age and gender. Since none were identified, we used the simple correlation analysis here for consistency with Test 2.

References

  1. Amos W et al (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond Ser B Biol Sci 268:2021–2027

  2. Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665

  3. Armstrong DP, Cassey P (2007) Estimating the effect of inbreeding on survival. Anim Conserv 10:487–492

  4. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031

  5. Banks SC, Knight EJ, Dubach J, Lindenmayer DB (2008) Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums. J Anim Ecol 77:1250–1256

  6. Beissinger SR, Wunderle JM, Meyers JM, Saether BE, Engen S (2008) Anatomy of a bottleneck: diagnosing factors limiting population growth in the Puerto Rican Parrot. Ecol Monogr 78:185–203

  7. Belov K, Lam MKP, Colgan DJ (2004) Marsupial MHC class II beta genes are not orthologous to the eutherian beta gene families. J Hered 95:338–345

  8. Brouwer L, Komdeur J, Richardson DS (2007) Heterozygosity-fitness correlations in a bottlenecked island species: a case study on the Seychelles warbler. Mol Ecol 16:3134–3144

  9. Burnham KP, Anderson DR (2003) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

  10. Chaix R, Cao C, Donnelly P (2008) Is mate choice in humans MHC-dependent? Plos Genet 4:e1000184. doi:10.1371/journal.pgen.1000184

  11. Coltman DW, Slate J (2003) Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971–983

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

  13. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259–1267

  14. Consuegra S, de Leaniz CG (2008) MHC-mediated mate choice increases parasite resistance in salmon. Proc R Soc B Biol Sci 275:1397–1403

  15. Coulson TN, et al. (1998) Microsatellites reveal inbreeding depression and heterosis in red deer. Proc R Soc Lond Ser B Biol Sci 265:489–495

  16. Crone EE (2001) Is survivorship a better fitness surrogate than fecundity? Evolution 55:2611–2614

  17. Dewoody YD, Dewoody JA (2005) On the estimation of genome wide heterozygosity using molecular markers. J Hered 96:85–88

  18. Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc R Soc Lond Ser B Biol Sci 264:127–132

  19. Fletcher RJ, Koford RR, Seaman DA (2006) Critical demographic parameters for declining songbirds breeding in restored grasslands. J Wildl Manag 70:145–157

  20. Forsberg LA, Dannewitz J, Petersson E, Grahn M (2007) Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout—females fishing for optimal MHC dissimilarity. J Evol Biol 20:1859–1869

  21. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723

  22. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

  23. Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114

  24. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474

  25. Hansson B, Westerberg L (2008) Heterozygosity-fitness correlations within inbreeding classes: local or genome-wide effects? Conserv Genet 9:73–83

  26. Hansson B, Bensch S, Hasselquist D, Akesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc R Soc Lond Ser B Biol Sci 268:1287–1291

  27. Hansson B, Westerdahl H, Hasselquist D, Akesson M, Bensch S (2004) Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers? Evolution 58:870–879

  28. Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109

  29. Heppell SS, Caswell H, Crowder LB (2000) Life histories and elasticity patterns: perturbation analyses for species with minimal demographic data. Ecology 65:4–665

  30. Holland OJ, Cowan PE, Gleeson DM, Chamley LW (2008) High variability in the MHC class II DA beta chain of the brushtail possum (Trichosurus vulpecula). Immunogenetics 60:775–781

  31. Jacob S, McClintock MK, Zelano B, Ober C (2002) Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat Genet 30:175–179

  32. Jamieson IG, Tracy LN, Fletcher D, Armstrong DP (2007) Moderate inbreeding depression in a reintroduced population of North Island robins. Anim Conserv 10:95–102

  33. Kappes D, Strominger JL (1988) Human class II major histocompatibility complex genes and proteins. Annu Rev Biochem 57:991–1028

  34. Kruuk LEB, Sheldon BC, Merila J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond Ser B Biol Sci 269:1581–1589

  35. Kurtz J et al (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond Ser B Biol Sci 271:197–204

  36. Lam MKP, Hickson RE, Cowan PE, Cooper DW (2000) A major histocompatibility (MHC) microsatellite locus in brushtail possums (Trichosurus vulpecula). J Vet Res 4:139–141

  37. Lebreton JD, Pradel R, Clobert J (1993) The statistical-analysis of survival in animal populations. Trends Ecol Evol 8:91–95

  38. Lindenmayer DB, Welsh A, Donnelly CF, Meggs RA (1996) Use of nest trees by the mountain brushtail possum (Trichosurus caninus) (Phalangeridae:Marsupialia). 1. Number of occupied trees and frequency of tree use. Wildl Res 23:343–361

  39. Lindenmayer DB, Welsh A, Donnelly CF (1997) Use of nest trees by the mountain brushtail possum (Trichosurus caninus) (Phalangeridae: Marsupialia). III. Spatial configuration and co-occupancy of nest trees. Wildl Res 24:661–677

  40. Lindenmayer DB, Lacy RC, Viggers KL (1998) Modelling survival and capture probabilities of the Mountain Brushtail Possum (Trichosurus caninus) in the forests of south-eastern Australia using trap-recapture data. J Zool 245:1–13

  41. Lindenmayer DB, Dubach J, Viggers KL (2002) Geographic dimorphism in the mountain brushtail possum (Trichosurus caninus): the case for a new species. Aust J Zool 50:369–393

  42. Luikart G, Pilgrim K, Visty J, Ezenwa VO, Schwartz MK (2008) Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep. Biol Lett 4:228–231

  43. Madsen T, Ujvari B (2006) MHC class I variation associates with parasite resistance and longevity in tropical pythons. J Evol Biol 19:1973–1978

  44. Markert JA, Grant PR, Grant BR, Keller LF, Coombs JL, Petren K (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin’s ground finches (Geospiza fortis and G-scandens). Heredity 92:306–315

  45. Martin JK (2006) Den-use and home-range characteristics of bobucks, Trichosurus cunninghami, resident in a forest patch. Aust J Zool 54:225–234

  46. Ottova E, Simkova A, Morand S (2007) The role of major histocompatibility complex diversity in vigour of fish males (Abramis brama L.) and parasite selection. Biol J Linn Soc 90:525–538

  47. Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc Natl Acad Sci USA 95:3714–3719

  48. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

  49. Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

  50. Pemberton JM (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615

  51. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

  52. Pitcher TE, Neff BD (2006) MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol Ecol 15:2357–2365

  53. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43:258–275

  54. Raymond M, Rousset F (1995) Genepop (version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249

  55. Rijks JM, Hoffman JI, Kuiken T, Osterhaus A, Amos W (2008) Heterozygosity and lungworm burden in harbour seals (Phoca vitulina). Heredity 100:587–593

  56. Saether BE, Bakke O (2000) Avian life history variation and contribution of demographic rates to the population growth rate. Ecology 81:642–653

  57. Sandercock BK (2006) Estimation of demographic parameters from live encounter data: a summary review. J Wildl Manage 70:1504–1520

  58. Sandercock BK, Jensen WE, Williams CK, Applegate RD (2008) Demographic sensitivity of population change in northern bobwhite. J Wildl Manage 72:970–982

  59. Seamans ME, Gutierrez RJ (2007) Sources of variability in spotted owl population growth rate: testing predictions using long-term mark-recapture data. Oecologia 152:57–70

  60. Seebeck JH, Warneke RM, Baxter BJ (1984) Diet of the bobuck, Trichosurus caninus (Ogilby) (Marsupialia: Phalangeridae) in a mountain forest in Victoria. In: Smith AP, Hume ID (eds) Possums and gliders. Surrey Beatty, Sydney, pp 145–154

  61. Slate J et al (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 95:255–266

  62. Taylor AC, Cooper DW (1998) Microsatellite markers for the Phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula). Mol Ecol 7:1780–1782

  63. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

  64. Viggers KL (1996) Assessment of health, condition and the effects of parasites in the mountain brushtail possum. Ph.D. thesis, Australian National University, Canberra

  65. Wedekind C (2002) The MHC and body odors: arbitrary effects caused by shifts of mean pleasantness. Nat Genet 31:237

  66. Wedekind C, Furi S (1997) Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc R Soc Lond Ser B Biol Sci 264:1471–1479

  67. Wegner KM, Kalbe M, Milinski M, Reusch TBH (2008) Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype—art. no. 124. BMC Evol Biol 8:124

  68. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139

  69. Woelfing B, Traulsen A, Milinski M, Boehm T (2009) Does intra-individual major histocompatibility complex diversity keep a golden mean? Phil Trans R Soc B Biol Sci 364:117–128

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Acknowledgments

This work was supported by the Hermon Slade Foundation (grant 08-4), the Australian Research Council (project DP0984876) and the Commonwealth Environment Research Facility Applied Environmental Decision Analysis research hub. Thanks to Lachlan McBurney, Damian Michael, Chris Macgregor and Mason Crane for assistance in the field. The manuscript editor, Jörg Ganzhorn, and two anonymous referees provided constructive criticism of an earlier version of the manuscript.

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Correspondence to Sam C. Banks.

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Communicated by Jörg Ganzhorn.

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Banks, S.C., Dubach, J., Viggers, K.L. et al. Adult survival and microsatellite diversity in possums: effects of major histocompatibility complex-linked microsatellite diversity but not multilocus inbreeding estimators. Oecologia 162, 359–370 (2010). https://doi.org/10.1007/s00442-009-1464-0

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Keywords

  • Survival
  • Mark-recapture
  • Major histocompatibility complex
  • Assignment test
  • Parasite load