Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Adult survival selection in relation to multilocus heterozygosity and body size in a tropical bird species, the Zenaida dove, Zenaida aurita

Abstract

Both phenotypic and genetic quality can influence the survival of individuals through time, although their relative influences are rarely addressed simultaneously. Here we used capture–mark–recapture modelling to assess the influence of both multilocus heterozygosity (MLH) and body size on apparent adult survival in a tropical bird species, the Zenaida dove, Zenaida aurita, using a sample of 391 individuals genotyped at 11 microsatellites, while controlling for the effects of sex. No effect of body size on either adult survival or capture rate was found. In the best model, survival was a logit linear function of MLH, whereas detection probability was a sex-dependent logit linear function of the logarithm of field effort, increasing with time and affected by a random individual effect. Using a Bayesian approach, we found that MLH explained 1.14 % of the total deviance, as expected from theory and previous studies of heterozygosity-fitness correlations, with no evidence for local effects. However, results from capture–mark–recapture modelling indicated that expected longevity varied from 4.8 years in the least heterozygous individuals (MLH = 0.37) to 10.6 years in the most heterozygous ones (MLH = 1), thus suggesting that MLH had potentially a substantial effect on survival. We discuss our results in relation to current hypotheses about the origin of heterozygosity-fitness correlations.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Acquarone C, Cucco M, Malacarne G, Silvano F (2004) Temporary shift of body size in hooded crows Corvus corone cornix of NW Italy. Folia Zool 53:379–384

  2. Agudo R, Carrete M, Alcaide M, Rico C, Hiraldo F, Donazar JA (2012) Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird. Proc R Soc Lond B 279:3241–3249

  3. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petran N, Csaki F (eds) International Symposium on Information Theory. Akadémiai Kiadi, Budapest, pp 267–281

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

  5. Banks SC, Dubach J, Viggers KL, Lindenmayer DB (2010) Adult survival and microsatellite diversity in possums: effects of major histocompatibility complex-linked microsatellite diversity but not multilocus inbreeding estimators. Oecologia 162:359–370

  6. Barbraud C (2000) Natural selection on body size traits in a long-lived bird, the snow petrel, Pagodroma nivea. J Evol Biol 13:81–88

  7. Bertrand JAM, Bourgeois XYC, Delahaie B, Duval T, García-Jiménez R, Cornuault J, Heeb P, Milá B, Pujol B, Thébaud C (2014) Extremely reduced dispersal and gene flow in an island bird. Heredity 112:190–196

  8. Björklund M, Sennar JC (2001) Sex differences in survival selection in the serin, Serinus serinus. J Evol Biol 14:841–849

  9. Boag PT, Grant PR (1981) Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galápagos. Science 214:82–85

  10. Bodie JR, Semlitsch RD (2000) Size-specific mortality and natural selection in freshwater turtles. Copeia 3:732–739

  11. Bond J (1993) A field guide to the birds of the West Indies, 5th edn. Houghton Mifflin, Harcourt

  12. Brown CR, Brown MB (1998) Intense natural selection on body size and wing and tail asymmetry in cliff swallows during severe weather. Evolution 52:1461–1475

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

  14. Cain BA, Wandera B, Shawcross SG, Harris WE, Stevens-Wood B, Kemp SJ, Okita-Ouma B, Watts PC (2014) Sex-biased inbreeding effects on reproductive success and home range size of the critically endangered black rhinoceros. Cons Biol 28:594–603

  15. Carlson SM, Olsen EM, Vøllestad LA (2008) Seasonal mortality and the effect of body size: a review and an empirical test using the brown trout. Funct Ecol 22:663–673

  16. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18:2746–2765

  17. Choquet R, Rouan L, Pradel R (2009) Program E-SURGE: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations, book 3. Springer, Berlin, pp 847–868

  18. Clark JA (2009) Selective mortality of waders during severe weather. Bird Study 56:96–102

  19. Clobert J (1995) Capture–recapture and evolutionary ecology: a difficult wedding? J Appl Stat 22:989–1008

  20. Cooch EG, Cam E, Link W (2002) Occam’s shadow: levels of analysis in evolutionary ecology—where to next? J Appl Stat 29:19–48

  21. Davies JC, Rockwell RF, Cooke F (1988) Body-size variation and fitness components in lesser snow geese (Chen caerulescens caerulescens). Auk 105:639–648

  22. De Léon LF, Bermingham E, Podos J, Hendry AP (2010) Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin’s finches. Philos Trans R Soc B 365:1041–1052

  23. Dechaume-Moncharmont F-X, Monceau K, Cézilly F (2011) Sexing birds using discriminant function analysis: a critical appraisal. Auk 128:78–86

  24. Endler J (1986) Natural selection in the wild. Princeton University Press, Princeton

  25. Evans ML, Neff BD, Heath DD (2010) MHC-mediated local adaptation in reciprocally translocated Chinook salmon. Cons Genet 11:2333–2342

  26. Forcada J, Hoffman JI (2014) Climate change selects for heterozygosity in a declining fur seal population. Nature 511:462–465

  27. Fortsmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B (2012) Heterozygosity–fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Mol Ecol 21:3237–3249

  28. Garroway CJ, Radersma R, Sepil I, Santure AW, De Cauwer I, Slate J, Sheldon BC (2013) Fine-scale genetic structure in a wild bird population: the role of limited dispersal and environmentally based selection as causal factors. Evolution 67:3488–3500

  29. Geraci J, Béchet A, Cézilly F, Ficheux S, Baccetti N, Samraoui B, Wattier R (2012) Greater flamingo colonies around the Mediterranean form a single interbreeding population and share a common history. J Avian Biol 43:341–354

  30. Gillingham MAF, Cézilly F, Wattier R, Béchet A (2013) Evidence for an association between post-fledging dispersal and microsatellite multilocus heterozygosity in a large population of greater flamingos. PLoS One 8(11):e81118. doi:10.1371/journal.pone.0081118

  31. Gimenez O, Choquet R (2010) Individual heterogeneity in studies on marked animals using numerical integration: capture–recapture mixed models. Ecology 91:951–957

  32. Gimenez O, Viallefont A, Charmantier A, Pradel R, Cam E, Brown CR, Covas R, Gaillard JM (2008) The risk of flawed inference in evolutionary studies when detectability is less than one. Am Nat 172:441–448

  33. Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186

  34. Hall KSS, Ryttman H, Fransson T, Stolt B-O (2004) Stabilising selection on wing length in reed warblers Acrocephalus scirpaceus. J Avian Biol 35:7–12

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

  36. Harrison XA, Bearhop S, Inger R, Colhoun K, Gudmundsson GA, Hodgson D, McElwaine G, Tregenza T (2011) Heterozygosity-fitness correlations in a migratory bird: an analysis of inbreeding and single-locus effects. Mol Ecol 20:4786–4795

  37. Herdegen M, Nadachowska-Brzyska K, Konowalik A, Babik W, Radwan J (2013) Heterozygosity, sexual ornament and body size in the crested newt. J Zool 291:146–153

  38. Herdegen M, Dudka K, Radwan J (2014) Heterozygosity and orange coloration are associated in the guppy (Poecilia reticulata). J Evol Biol 27:220–225

  39. Hoffman JI, Hanson N, Forcada J, Trathan PN, Amos W (2010) Getting long in the tooth: a strong positive correlation between canine size and heterozygosity in Antarctic fur seals Arctocephalus gazella. J Hered 101:527–538

  40. Hoffman JL, Simpson F, David P, Rijks JM, Kuiken T, Thorne MAS, Lacyg RC, Dasmahapatrah KK (2014) High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci USA 111:3775–3780

  41. Johnson DW, Hixon MA (2010) Ontogenetic and spatial variation in size-selective mortality of a marine fish. J Evol Biol 23:724–737

  42. Jones G (1987) Selection against large size in the sand martin Riparia riparia during a dramatic population crash. Ibis 129:274–280

  43. Kardos M, Allendorf FW, Lukart G (2013) Evaluating the role of inbreeding depression in heterozygosity-fitness correlations: how useful are tests for identity disequilibrium? Mol Ecol Res 14:519–530

  44. Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. Bioscience 57:561–571

  45. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CH, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

  46. Kloch A, Baran K, Buczek M, Konarzewski M, Radwan J (2013) MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus. Evol Ecol 27:635–653

  47. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

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

  49. 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

  50. Milá B, Warren BH, Heeb P, Thébaud C (2010) The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus). BMC Evol Biol 10:158

  51. Miller JM, Coltman DW (2014) Assessment of identity disequilibrium and its relation to empirical heterozygosity fitness correlations: a meta-analysis. Mol Ecol 23:1899–1909

  52. Miller JM, Malenfant RM, David P, Davis CS, Poissant J, Hogg JT, Festa-Bianchet M, Coltman DW (2014) Estimating genome-wide heterozygosity: effects of demographic history and marker type. Heredity 112:240–247

  53. Milner JM, Albon SD, Illius AW, Pemberton JM, Clutton-Brock TH (1999) Repeated selection of morphometric traits in the Soay sheep on St Kilda. J Anim Ecol 68:472–488

  54. Monaghan P, Metcalfe NB (1986) On being the right size: natural selection and body size in the herring gull. Evolution 40:1096–1099

  55. Monceau K, Gaillard M, Harrang E, Santiago-Alarcon D, Parker P, Cézilly F, Wattier R (2009) Twenty-three polymorphic microsatellite markers for the Caribbean endemic Zenaida dove, Zenaida aurita, and its conservation in related Zenaida species. Cons Genet 10:1577–1581

  56. Monceau K, Wattier R, Dechaume-Moncharmont F-X, Motreuil S, Cézilly F (2011) Territoriality vs. flocking in the Zenaida dove, Zenaida aurita: resource polymorphism revisited using morphological and genetic analyses. Auk 128:15–25

  57. Monceau K, Wattier R, Dechaume-Moncharmont F-X, Dubreuil C, Cézilly F (2013a) Heterozygosity-fitness correlations in adult and juvenile Zenaida doves, Zenaida aurita. J Heredity 104:47–56

  58. Monceau K, Cézilly F, Moreau J, Motreuil S, Wattier R (2013b) Genetic and morphological evidence suggests rapid differentiation between island populations of a Caribbean endemic bird species, the Zenaida dove, Zenaida aurita. PLoS One 8:e82189. doi:10.1371/journal.pone.0082189

  59. Munch SB, Mangel M, Conover DO (2003) Quantifying natural selection on body size from field data with an application to winter mortality in Menidia menidia. Ecology 84:2168–2177

  60. Nolan PM, Hill GE, Stoehr AM (1998) Sex, size, and plumage redness predict house finch survival in an epidemic. Proc R Soc B 265:961–965

  61. Plummer M (2003) JAGS: a program for the analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), Vienna. ISSN 1609-395X

  62. Potti J, Canal D, Serrano D (2013) Lifetime fitness and age-related female ornament signalling: evidence for survival and fecundity selection in the pied flycatcher. J Evol Biol 26:1445–1457

  63. Quinard A, Cézilly F (2012) Sex roles during conspecific territorial defence in the Zenaida dove, Zenaida aurita. Anim Behav 83:47–54

  64. Quinard A, Dechaume-Moncharmont FX, Cézilly F (2014) Pairing patterns in relation to body size, genetic similarity and multilocus heterozygosity in a tropical monogamous bird species. Behav Ecol Sociobiol 68:1723–1731

  65. Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402

  66. Redfield JA (1974) Genetics and selection at the Ng locus in blue grouse (Dendragapus obscurus). Heredity 33:69–78

  67. Reznick DN, Butler MJ IV, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata). 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660

  68. Rhodes OE, Smith LM, Smith MH (1996) Relationships between genetic variation and body size in wintering mallards. Auk 113:339–345

  69. Rivera-Milan FF (1996) Nest density and success of columbids in Puerto Rico. Condor 98:100–113

  70. Rivera-Milan FF (2001) Transect surveys of columbid nests on Puerto Rico, Vieques, and Culebra Islands. Condor 103:332–342

  71. Rivera-Milan FF, Schafner FC (2002) Demography of Zenaida doves on Cayo del Agua, Culebra, Puerto Rico. Condor 104:587–597

  72. Rotella JJ, Clark RG, Afton AD (2003) Survival of female lesser scaup: effect of body size, age, and reproductive effort. Condor 105:336–345

  73. Rousset F (2011) Genepop 4.1 for Windows/Linux/Mac OS X. http://kimura.univ-montp2.fr/~rousset/Genepop.htm

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

  75. Schaschl H, Suchentrunk F, Morris DL, Ben Slimen H, Smith S, Arnold W (2012) Sex-specific selection for MHC variability in Alpine chamois. BMC Evol Biol 12:20

  76. Schmeller DS, Schregel J, Veith M (2007) The importance of heterozygosity in a frog’s life. Naturwissenschaften 94:360–366

  77. Schulte-Hostedde A, Millar J, Gibbs L (2002) Female-biased sexual size dimorphism in the yellow-pine chipmunk (Tamias amoenus): sex-specific patterns of annual reproductive success and survival. Evolution 56:2519–2529

  78. Seber GAF (1982) The estimation of animal abundance and related parameters, 2nd edn. Griffin, London

  79. Sepil I, Lachish S, Sheldon BC (2013) Mhc-linked survival and lifetime reproductive success in a wild population of great tits. Mol Ecol 22:384–396

  80. Sol D, Elie M, Marcoux M, Chrostovsky E, Porcher C, Lefebvre L (2005) Ecological mechanisms of a resource polymorphism in Zenaida doves of Barbados. Ecology 86:2397–2407

  81. Su YS, Yajima M (2012) R2jags: a package for running jags from R. http://CRAN.R-project.org/package=R2jags

  82. Szulkin M, Bierne N, David P (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202–1217

  83. Vangestel C, Mergeay C, Dawson DA, Vandomme V, Lens L (2011) Spatial heterogeneity in genetic relatedness among house sparrows along an urban–rural gradient as revealed by individual-based analysis. Mol Ecol 20:4643–4653

  84. Weisberg S (1980) Applied linear regression. Wiley, New York

  85. Wetzel DP, Stewart IRK, Westneat DF (2012) Heterozygosity predicts clutch and egg size but not plasticity in a house sparrow population with no evidence of inbreeding. Mol Ecol 21:406–420

  86. Wiggins DA (1991) Natural selection on body size and laying date in the tree swallow. Evolution 45:1169–1174

  87. Wiley JW (1991) Ecology and behavior of the Zenaida dove. Ornithol Neotrop 2:49–75

  88. Winne CT, Willson JD, Gibbons JW (2010) Drought survival and reproduction impose contrasting selection pressures on maximum body size and sexual size dimorphism in a snake, Seminatrix pygaea. Oecologia 162:913–922

  89. Worley K, Collet J, Spurgin LG, Cornwallis C, Pizzari T, Richardson DS (2010) MHC heterozygosity and survival in red junglefowl. Mol Ecol 19:3064–3075

Download references

Acknowledgments

We would like to thank Joris Bertrand and one anonymous referees for very helpful comments. We are grateful to Mr Steve Devonish, Director of the Natural Heritage Department, for granting us the permission to capture and ring Zenaida Doves in Barbados, Nicole Atherley, Laurent Brucy, Carla Daniel, Marc Lavoie, Karine Monceau and Jérôme Moreau for help in catching and banding birds, and Christine Dubreuil and Maria Gaillard for help in genotyping. The study was funded by the Agence Nationale pour la Recherche (Programme Blanc Monogamix), the Institut Universitaire de France, and the Conseil Régional de Bourgogne. A. Q. was supported by a doctoral grant from the Ministère de l’Enseignement Supérieur et de la Recherche. We thank Jaume Forcada for very useful comments on an earlier version of the manuscript. The authors declare no conflict of interest.

Author contribution statement

F. C. and R. P. conceived and designed the study. F. C., A. Q. and S. M. collected the data. F. C., A. Q. and R. P. analysed the data. F. C., A. Q. and R. P. wrote the manuscript.

Author information

Correspondence to Frank Cézilly.

Additional information

Communicated by Indrikis Krams.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cézilly, F., Quinard, A., Motreuil, S. et al. Adult survival selection in relation to multilocus heterozygosity and body size in a tropical bird species, the Zenaida dove, Zenaida aurita . Oecologia 180, 127–136 (2016). https://doi.org/10.1007/s00442-015-3466-4

Download citation

Keywords

  • Demography
  • Heterozygosity-fitness correlations
  • Capture–mark–recapture modelling
  • Evolutionary ecology
  • Phenotype