Abstract
The relative influence of genetic and phenotypic quality on pairing status and mating patterns in socially monogamous species remains poorly documented. We studied social status and pairing patterns in relation to genetic similarity and multilocus heterozygosity (MLH) estimates from 11 microsatellite markers, and both tarsus length and wing chord (as a measure of competitive ability in territorial defence) in a socially monogamous tropical bird species where individuals defend territories year-round, alone or in pairs, the Zenaida dove, Zenaida aurita. Tarsus length and wing chord did not differ between unpaired territorial birds and paired ones in either sex, whereas paired females, but not paired males, tended to be more heterozygous than unpaired ones. Among 84 pairs, we found no evidence for assortative mating for tarsus length, wing chord, MLH or genetic similarity. However, within pairs, male wing chord was positively related to female MLH and female tarsus length was positively related to male MLH, with no evidence for local effects, suggesting assortative mating by individual quality. Although the observed pattern of mating in Zenaida doves may be the product of mutual mate choice, further assessment of this hypothesis requires direct investigation of both mating preference in each sex and lifetime reproductive success in relation to body size and MLH.
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References
Alberico JAR, Reed JM, Oring LW (1992) Nonrandom philopatry of sibling spotted sandpipers Actitis macularia. Ornis Scand 23:504–508
Alho JS, Välimäki K, Merilä J (2010) Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity-heterozygosity correlation. Mol Ecol Resour 10:720–722
Alonso H, Matias R, Granadeiro JP, Catry P (2009) Moult strategy of Cory’s shearwaters Calonectris diomedea borealis: the influence of colony location, sex and individual breeding status. J Ornithol 150:329–337
Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265:445–450
Aparicio JM (2011) The paradox of the resolution of the lek paradox based on mate choice for heterozygosity. Anim Behav 81:1271–1279
Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665
Barta Z, McNamara JM, Houston AI, Weber TP, Hedenström A, Feró O (2006) Optimal moult strategies in migratory birds. Philos Trans R Soc Lond B 363:211–229
Bateson M, Healy SD (2005) Comparative evaluation and its implication for mate choice. Trends Ecol Evol 20:659–664
Bond J (1993) A field guide to the birds of the West Indies. Houghton Mifflin Harcourt, Boston
Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006) Complex Mhc-based mate choice in a wild passerine. Proc R Soc Lond B 273:1111–1116
Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65
Cézilly F (2004) Assortative mating. In: Mark Bekoff (ed) Encyclopedia of animal behavior Greenwood Pres, Westport, pp 876-881
Cézilly F, Keddar I (2012) Vigilance and food intake rate in paired and solitary Zenaida doves Zenaida aurita. Ibis 154:161–166
Cézilly F, Boy V, Tourenq C, Johnson AR (1997) Age-assortative pairing in the Greater Flamingo, Phoenicopterus ruber roseus. Ibis 139:331–336
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
Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68:1229–1238
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487
Dechaume-Moncharmont FX, Monceau K, Cézilly F (2011) Sexing birds using discriminant function analysis: a critical appraisal. Auk 126:78–86
Dechaume-Moncharmont FX, Freychet M, Motreuil S, Cézilly F (2013) Female mate choice in convict cichlids is transitive and consistent with a self-referent directional rule. Front Zool 10:69
Delestrade A (2001) Sexual size dimorphism and positive assortative mating in Alpine choughs (Pyrrhocoraxg raculus). Auk 118:553–556
Echeverry-Galvis MA, Hau M (2012) Molt–breeding overlap alters molt dynamics and behavior in zebra finches, Taeniopygia guttata castanotis. J Exp Biol 215:1957–1964
Einoder LD, Page B, Goldsworthy SD (2008) Sexual size dimorphism and assortative mating in the short-tailed shearwater Puffinus tenuirostris. Mar Ornithol 36:167–173
Faivre B, Préault M, Théry M, Secondi J, Patris B, Cézilly F (2001) Breeding strategy and morphological characters in an urban population of blackbirds, Turdus merula. Anim Behav 61:969–974
Fasola M, Zhang YM, Zhao DQ, Dong YH, Wang H (2001) Age-assortative mating related to reproductive success in Black-crowned Night Herons. Waterbirds 24:272–276
Fawcett TW, Johnstone RA (2003) Mate choice in the face of costly competition. Behav Ecol 14:771–779
Foster M (1974) A model to explain molt-breeding overlap and clutch size in some tropical birds. Evolution 28:82–190
Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV (2003) Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 12:3077–3083
García-Navas V, Ortego J, Sanz JJ (2009) Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice. Proc R Soc Lond B 276:2931–2940
Ginn HB, Melville DS (1983) Moult in birds. BTO Guide 19, Tring, UK
Grant PR, Grant BR (2008) Pedigrees, assortative mating and speciation in Darwin’s finches. Proc R Soc Lond B 275:661–668
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Grilli MG, Montalti D (2010) On the study of the birds’ plumage: the case of the Eared Dove (Zenaida auriculata). Rev Brasil Ornitol 18:341–343
Haggerty TM (2006) Sexual size dimorphism and assortative mating in Carolina Wrens. J Field Ornithol 77:259–265
Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474
Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Helfenstein F, Danchin E, Wagner RH (2004) Assortative mating and sexual size dimorphism in Black-legged Kittiwakes. Waterbirds 27:350–354
Hemborg C, Merilä J (1998) A sexual conflict in collared flycatchers. Proc R Soc Lond B 265:2003–2007
Herdegen M, Nadachowska-Brzyska K, Konowalik A, Babik W, Radwan J (2013) Heterozygosity, sexual ornament and body size in the crested newt. J Zool 291:16–153
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
Holveck M-J, Riebel K (2010) Low-quality females prefer low-quality males when choosing a mate. Proc R Soc Lond B 277:153–160
Husseneder C, Simms DM (2008) Size and heterozygosity influence partner selection in the Formosan subterranean termite. Behav Ecol 19:764–773
Jawor JM, Linville SU, Beall SM, Breitwisch R (2003) Assortative mating by multiple ornaments in northern cardinals (Cardinalis cardinalis). Behav Ecol 14:515–520
Johnson SG, Johnston RF (1989) A multifactorial study of variation in interclutch interval and annual reproductive success in the feral pigeon, Columbia livia. Oecologia 80:87–92
Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391
Jones IL, Hunter FM (1993) Mutual mate choice in a monogamous seabird. Nature 362:238–239
Juola FA, Dearborn DC (2012) Sequence-based evidence for major histocompatibility complex-disassortative mating in a colonial seabird. Proc R Soc Lond B 279:153–162
Kardos M, Allendorf FW, Luikart G (2014) Evaluating the role of inbreeding depression in heterozygosity-fitness correlations: how useful are tests for indentity disequilibrium? Mol Ecol Resour 14:519–530
Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Adv Stud Behav 37:189–278
Knafler GJ, Clark JA, Boersma PD, Bouzat JL (2012) MHC diversity and mate choice in the Magellanic Penguin, Spheniscus magellanicus. J Hered 103:759–768
Ledwon M (2011) Sexual size dimorphism, assortative mating and sex identification in the whiskered tern Chlidonias hybrida. Ardea 99:191–198
Lovette IJ, Seutin G, Ricklefs RE, Bermingham E (1999) The assembly of an island fauna by natural invasion: sources and temporal patterns in the avian colonization of Barbados. Biol Inv 1:33–41
Macedo RH, Karubian J, Webster MS (2008) Extrapair paternity and sexual selection in socially monogamous birds: are tropical birds different? Auk 125:769–777
Marzluff JM, Balda RP (1988) Pairing patterns and fitness in a free-ranging population of pinyon jays: what do they reveal about mate choice? Condor 90:201–213
Matthysen E, Van de Casteele T, Adriaensen F (2005) Do sibling tits (Parus major, P. caeruleus) disperse over similar distances and in similar directions? Oecologia 143:301–307
Mays HL Jr, Alrecht T, Liu M, Hill GE (2008) Female choice for genetic complementarity in birds: a review. Genetica 134:147–158
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. Conserv Genet 10:1577–1581
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
Monceau K, Cézilly F, Moreau J, Motreuil S, Wattier R (2013a) 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
Monceau K, Wattier R, Dechaume-Moncharmont F-X, Dubreuil C, Cézilly F (2013b) Heterozygosity-fitness correlations in adult and juvenile Zenaida doves, Zenaida aurita. J Hered 104:47–56
Moreno-Rueda G (2006) Sexual size dimorphism and assortative mating for morphological traits in Passer domesticus. J Ethol 24:227–230
Mulard H, Danchin E, Talbot SL, Ramey AM, Hatch SA, White JF, Helfenstein F, Wagner RH (2009) Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird. BMC Evol Biol 9:147
Olano-Marin J, Mueller JC, Kempenaers B (2011) Correlations between heterozygosity and reproductive success in the blue tit (Cyanistes caeruleus): an analysis of inbreeding and single locus effects. Evolution 20:4028–4041
Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007) Egg production and individual genetic diversity in lesser kestrels. Mol Ecol 16:2383–2392
Ortego J, Calabuig G, Bonal R, Munoz A, Aparicio JM, Cordero PJ (2009) Temporal variation of heterozygosity-based assortative mating and related benefits in a lesser kestrel population. J Evol Biol 22:2488–2495
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43:258–275
Quinard A, Cézilly F (2012) Sex roles during conspecific territorial defence in the Zenaida dove, Zenaida aurita. Anim Behav 83:47–54
Reaney LT (2009) Female preference for male phenotypic traits in a fiddler crab: do female use absolute or comparative evaluation? Anim Behav 77:139–143
Regosin JV, Pruett-Jones S (2001) Sexual selection and tail-length dimorphism in scissor-tailed flycatchers. Auk 118:167–175
Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674
Rousset F (2011) Genepop 4.1 for Windows/Linux/Mac OS X, http://kimura.univ-montp2.fr/~rousset/Genepop.htm
Row KMC, Weatherhead PJ (2011) Assortative mating in relation to plumage traits shared by male and female American Robins. Condor 113:881–889
Shaner P-J, Chen Y-R, Li J-W, Kolbe JJ, Lin S-M (2013) Sex-specific correlations of individual heterozygosity, parasite load, and scalation asymmetry in a sexually dichromatic lizard. PLoS One 8:e56720
Sol D, Elie M, Marcoux M, Chrostovsky E, Porcher C, Lefebvre L (2005) Ecological mechanisms of resource polymorphism in Zenaida doves of Barbados. Ecology 86:2397–2407
Sommer S (2005) MHC-dependent mate choice in a monogamous rodent. Behav Ecol Sociobiol 58:181–189
Stutchbury BJM, Morton ES (2008) Recent advances in the behavioral ecology of tropical birds. Wilson J Ornithol 120:26–37
Svensson E, Nilsson JA (1997) The trade-off between moult and parental care: a sexual conflict in the blue tit? Behav Ecol 8:92–98
Szulkin M, Bierne N, David P (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202–1217
Thünken T, Meuthen D, Bakker TCM, Baldauf SA (2012) A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice. Proc R Soc Lond B 279:2959–2964
Tidemann SC, Woinarski JCZ (1994) Moult characteristics and breeding seasons of Gouldian Erythrura gouldiae. Masked Poephila personata and Long-tailed Finches P. acuticauda in savannah woodland in the Northern Territory. Emu 94:46–52
Tomiuk J, Stauss M, Segelbacher G, Fietz J, Kömpf J, Bachmann L (2007) Female genetic heterogeneity affects the reproduction of great tits (Parus major L., 1758) in low-quality woodlands. J Zool Syst Evol Res 45:144–150
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage. Mol Ecol 9:1013–1027
van Oosterhout C, Hutchinson WF, Wills DPM, Shirley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wagner RH (1999) Sexual size dimorphism and assortative mating in razorbills (Alca torda). Auk 116:542–544
Weimerskirch H (1991) Sex-specific differences in moult strategy in relation to breeding in the wandering albatross. Condor 93:731–737
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
Wiley JW (1991) Ecology and behavior of the Zenaida dove. Ornitol Neotrop 2:49–75
Wyndham E (1986) Length of birds’ breeding seasons. Am Nat 128:155–164
Acknowledgments
We thank three anonymous referees for very helpful comments on an earlier version. We are particularly grateful to Mr. Steve Devonish, Director of Natural Heritage, and Kim Downes Agard for granting us the permission to capture and ring Zenaida doves and to Cyril Bhola for hospitality. We thank Karine Monceau, Nicole Atherley, Laurent Brucy, Carla Daniel, Jérôme Moreau and Sébastien Motreuil, for their help in catching and banding birds, and Christine Dubreuil and Maria Gaillard for their help in genotyping. Patrice David provided very helpful comments on the manuscript. The study was funded by the Agence Nationale pour la Recherche (ANR, Programme Blanc “Monogamix”) and the Conseil Régional de Bourgogne. AQ was supported by a doctoral grant from the Ministère de l’Enseignement Supérieur et de la Recherche.
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The authors declare that they have no conflict of interest.
Ethical standards
Research was conducted under permit from the National Heritage Department (Division of Ministry of Environment and Drainage of Barbados). The experiments comply with the current laws of Barbados.
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Quinard, A., Dechaume-Moncharmont, FX. & Cézilly, F. Pairing patterns in relation to body size, genetic similarity and multilocus heterozygosity in a tropical monogamous bird species. Behav Ecol Sociobiol 68, 1723–1731 (2014). https://doi.org/10.1007/s00265-014-1780-1
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DOI: https://doi.org/10.1007/s00265-014-1780-1