BACKGROUND: Female promiscuity is highly variable among birds, and particularly among songbirds. Comparative work has identified several patterns of covariation with social, sexual, ecological and life history traits. However, it is unclear whether these patterns reflect causes or consequences of female promiscuity, or if they are byproducts of some unknown evolutionary drivers. Moreover, factors that explain promiscuity at the deep nodes in the phylogenetic tree may be different from those important at the tips, i.e. among closely related species. Here we examine the relationships between female promiscuity and a broad set of predictor variables in a comprehensive data set (N = 202 species) of Passerides songbirds, which is a highly diversified infraorder of the Passeriformes exhibiting significant variation in female promiscuity. RESULTS: Female promiscuity was highly variable in all major clades of the Passerides phylogeny and also among closely related species. We found several significant associations with female promiscuity, albeit with fairly small effect sizes (all R2 ≤ 0.08). More promiscuous species had: 1) less male parental care, particularly during the early stages of the nesting cycle (nest building and incubation), 2) more short-term pair bonds, 3) greater degree of sexual dichromatism, primarily because females were drabber, 4) more migratory behaviour, and 5) stronger pre-mating sexual selection. In a multivariate model, however, the effect of sexual selection disappeared, while the other four variables showed additive effects and together explained about 16% of the total variance in female promiscuity. Female promiscuity showed no relationship with body size, life history variation, latitude or cooperative breeding. CONCLUSIONS: We found that multiple traits were associated with female promiscuity, but these associations were generally weak. Some traits, such as reduced parental care in males and more cryptic plumage in females, might even be responses to, rather than causes of, variation in female promiscuity. Hence, the high variation in female promiscuity among Passerides species remains enigmatic. Female promiscuity seems to be a rapidly evolving trait that often diverges between species with similar ecologies and breeding systems. A future challenge is therefore to understand what drives within-lineage variation in female promiscuity over microevolutionary time scales.

A P Leventis Ornithological Research Institute University of Jos Jos Nigeria

Biotechnology Unit Department of Biological Sciences Elizade University P M B 002 Ilara Mokin Ondo State Nigeria

Center for Macroecology Evolution and Climate Natural History Museum of Denmark University of Copenhagen Universitetsparken 15 DK 2100 Copenhagen Denmark

Centre for Ecological and Evolutionary Synthesis Department of Biosciences University of Oslo P O Box 1066 Blindern NO 0316 Oslo Norway

Department of Zoology Charles University Prague Viničná 7 CZ 12844 Prague Czech Republic

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic v v i Květná 8 CZ 67502 Brno Czech Republic

Macaronesian Institute of Field Ornithology C Elias Ramos Gonzalez 5 3 H 38001 Santa Cruz de Tenerife Canary Islands Spain

Natural History Museum University of Oslo P O Box 1172 Blindern NO 0318 Oslo Norway

Norwegian Institute for Nature Research P O Box 5685 Torgarden NO 7485 Trondheim Norway

See more in PubMed

Griffith SC, Owens IPF, Thuman KA. Extrapair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol. 2002;11(11):2195–2212. doi: 10.1046/j.1365-294X.2002.01613.x. PubMed DOI

Arct A, Drobniak SM, Cichoń M. Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies. Behav Ecol. 2015;26(4):959–968. doi: 10.1093/beheco/arv004. DOI

Arnqvist G, Kirkpatrick M. The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extra-pair copulation behavior in females. Am Nat. 2005;165(supplement):S26–S37. doi: 10.1086/429350. PubMed DOI

Forstmeier W, Nakagawa S, Griffith SC, Kempenaers B. Female extra-pair mating: adaptation or genetic constraint? Trends Ecol Evol. 2014;29(8):456–464. doi: 10.1016/j.tree.2014.05.005. PubMed DOI

Wan D, Chang P, Yin J. Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds. Acta Ecol Sin. 2013;33(3):158–166. doi: 10.1016/j.chnaes.2013.03.006. DOI

Hsu Y-H, Schroeder J, Winney I, Burke T, Nakagawa S. Are extra-pair males different from cuckolded males? A case study and a meta-analytic examination. Mol Ecol. 2015;24:1558–1571. doi: 10.1111/mec.13124. PubMed DOI

Arnold KE, Owens IPF. Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc R Soc B. 2002;269:1263–1269. doi: 10.1098/rspb.2002.2013. PubMed DOI PMC

Bennett PM, Owens IPF. Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford: Oxford University Press; 2002.

Petrie M, Kempenaers B. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol. 1998;13(2):52–58. doi: 10.1016/S0169-5347(97)01232-9. PubMed DOI

Birkhead TR, Møller AP. Sperm competition in birds. Evolutionary causes and consequences. London: Academic; 1992.

Westneat DF, Sherman PW, Morton ML. The ecology and evolution of extra-pair copulations in birds. Curr Ornithol. 1990;7:331–369.

Westneat DF, Sherman PW. Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol. 1997;41(4):205–215. doi: 10.1007/s002650050381. DOI

Brouwer L, van de Pol M, Aranzamendi NH, Bain G, Baldassarre DT, Brooker LC, Brooker MG, Colombelli-Négrel D, Enbody E, Gielow K, Hall ML, Johnson AE, Karubian J, Kingma SA, Kleindorfer S, Louter M, Mulder RA, Peters A, Pruett-Jones S, Tarvin KA, Thrasher DJ, Varian-Ramos CW, Webster MS, Cockburn A. Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family. Mol Ecol. 2017;26(23):6717–6729. doi: 10.1111/mec.14385. PubMed DOI

Double MC, Cockburn A. Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc Royal Soc B. 2000;267:465–470. doi: 10.1098/rspb.2000.1023. PubMed DOI PMC

Lifjeld JT, Robertson RJ. Female control of extra-pair fertilization in tree swallows. Behav Ecol Sociobiol. 1992;31:89–96. doi: 10.1007/BF00166341. DOI

Neudorf DL, Stutchbury BJ, Piper WH. Covert extraterritorial behavior of female hooded warblers. Behav Ecol. 1997;8(6):595–600. doi: 10.1093/beheco/8.6.595. DOI

Wojczulanis-Jakubas K, Jakubas D, Øigarden T, Lifjeld JT. Extrapair copulations are frequent but unsuccessful in a highly colonial seabird, the little auk, Alle alle. Anim Behav. 2009;77(2):433–438. doi: 10.1016/j.anbehav.2008.10.019. DOI

Hasselquist D, Sherman PW. Social mating systems and extrapair fertilizations in passerine birds. Behav Ecol. 2001;12(4):457–466. doi: 10.1093/beheco/12.4.457. DOI

Cornwallis CK, West SA, Davis KE, Griffin AS. Promiscuity and the evolutionary transition to complex societies. Nature. 2010;466(7309):969–972. doi: 10.1038/nature09335. PubMed DOI

Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B. Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature. 2002;419(6907):613–615. doi: 10.1038/nature01104. PubMed DOI

Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT. Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett. 2005;1:389–392. doi: 10.1098/rsbl.2005.0376. PubMed DOI PMC

Gowaty PA. Multiple mating by females selects for males that stay: another hypothesis for social monogamy in passerine birds. Anim Behav. 1996;51(2):482–484. doi: 10.1006/anbe.1996.0052. DOI

Wink M, Dyrcz A. Mating systems in birds: a review of molecular studies. Acta Ornithol. 1999;34(2):91–109.

Stutchbury BJM, Morton ES. Behavioral ecology of tropical birds. San Diego: Academic; 2001.

Spottiswoode C, Møller AP. Extrapair paternity, migration, and breeding synchrony in birds. Behav Ecol. 2004;15(1):41–57. doi: 10.1093/beheco/arg100. DOI

Møller AP, Birkhead TR. Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol. 1993;33(4):261–268. doi: 10.1007/BF02027123. DOI

Møller AP. Male parental care, female reproductive success, and extrapair paternity. Behav Ecol. 2000;11(2):161–168. doi: 10.1093/beheco/11.2.161. DOI

Møller AP, Cuervo JJ. The evolution of paternity and paternal care in birds. Behav Ecol. 2000;11(5):472–485. doi: 10.1093/beheco/11.5.472. DOI

Birkhead TR, Møller AP. Monogamy and sperm competition in birds. In: Black JM, editor. Partnerships in birds: the study of monogamy. Oxford: Oxford University Press; 1996. pp. 323–343.

Schwagmeyer PL, St Clair RC, Moodie JD, Lamey TC, Schnell GD, Moodie MN. Species differences in male parental care in birds: a reexamination of correlates with paternity. Auk. 1999;116(2):487–503. doi: 10.2307/4089381. DOI

Owens IPF, Bennett PM. Ancient ecological diversification explains life-history variation among living birds. Proc R Soc B. 1995;261(1361):227–232. doi: 10.1098/rspb.1995.0141. DOI

Remeš V, Freckleton RP, Tökölyi J, Liker A, Székely T. The evolution of parental cooperation in birds. Proc Natl Acad Sci U S A. 2015;112(44):13603–13608. doi: 10.1073/pnas.1512599112. PubMed DOI PMC

del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E. Handbook of the birds of the world alive. In. Barcelona: Lynx Edicions; 2018.

Pienaar J, Ilany A, Geffen E, Yom-Tov Y. Macroevolution of life-history traits in passerine birds: adaptation and phylogenetic inertia. Ecol Lett. 2013;16(5):571–576. doi: 10.1111/ele.12077. PubMed DOI

Wiersma P, Muñoz-Garcia A, Walker A, Williams JB. Tropical birds have a slow pace of life. Proc Natl Acad Sci U S A. 2007;104(22):9340–9345. doi: 10.1073/pnas.0702212104. PubMed DOI PMC

Cracraft J. Avian higher-level relationships and classification. In: Dickinson EC, Christidis L, editors. The Howard and Moore Complete Checklist of the Birds of the World 4th edition, Vol 2. Eastbourne: Aves Press; 2014. pp. xvii–xxlv.

Kleven O, Bjerke B-A, Lifjeld JT. Genetic monogamy in the common crossbill (Loxia curvirostra) J Ornithol. 2008;149(4):651–654. doi: 10.1007/s10336-008-0291-0. DOI

Robertson BC, Degnan SM, Kikkawa J, Moritz CC. Genetic monogamy in the absence of paternity guards: the Capricorn silvereye, Zosterops lateralis chlorocephalaus, on Heron Island. Behav Ecol. 2001;12(6):666–673. doi: 10.1093/beheco/12.6.666. DOI

Brekke P, Wang J, Bennett PM, Cassey P, Dawson DA, Horsburgh GJ, Ewen JG. Postcopulatory mechanisms of inbreeding avoidance in the island endemic hihi (Notiomystis cincta) Behav Ecol. 2012;23(2):278–284. doi: 10.1093/beheco/arr183. DOI

Hill CE, Gjerdrum C, Elphick CS. Extreme levels of multiple mating characterize the mating system of the saltmarsh sparrow (Ammodramus caudacutus) Auk. 2010;127(2):300–307. doi: 10.1525/auk.2009.09055. DOI

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high troughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2):221–224. doi: 10.1093/molbev/msp259. PubMed DOI

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17(4):540–552. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI

Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772. doi: 10.1038/nmeth.2109. PubMed DOI PMC

Lerner H, Meyer M, James HF, Hofreiter M, Fleischer RC. Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr Biol. 2011;21(21):1838–1844. doi: 10.1016/j.cub.2011.09.039. PubMed DOI

Rambaut A, Suchard MA, Xie D, Drummond AJ. Tracer v. 1.6. 2014.

Macedo RH, Karubian J, Webster MS. Extrapair paternity and sexual selection in socially monogamous birds: are tropical birds different? Auk. 2008;125(4):769–777. doi: 10.1525/auk.2008.11008. DOI

Calhim S, Immler S, Birkhead TR. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One. 2007;2(5):e413. doi: 10.1371/journal.pone.0000413. PubMed DOI PMC

Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, Lope F, Hermosell I, Johannessen L, Kleven O, Marzal A, Mousseau T, Møller A, Robertson R, Rudolfsen G, Saino N, Vortman Y, Lifjeld J. Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol. 2013;67(2):301–309. doi: 10.1007/s00265-012-1450-0. DOI

Lifjeld JT, Laskemoen T, Kleven O, Albrecht T, Robertson RJ. Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One. 2010;5(10):e13456. doi: 10.1371/journal.pone.0013456. PubMed DOI PMC

Fitzpatrick JL, Baer B. Polyandry reduces sperm length variation in social insects. Evolution. 2011;65(10):3006–3012. doi: 10.1111/j.1558-5646.2011.01343.x. PubMed DOI

Varea-Sánchez M, Gómez Montoto L, Tourmente M, Roldan ERS. Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents. PLoS One. 2014;9(9):e108148. doi: 10.1371/journal.pone.0108148. PubMed DOI PMC

Kucera AC, Heidinger BJ. Avian semen collection by cloacal massage and isolation of DNA from sperm. J Vis Exp. 2018;132:e55324. PubMed PMC

Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT. Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution. 2009;63(9):2466–2473. doi: 10.1111/j.1558-5646.2009.00725.x. PubMed DOI

Sokal RR, Rohlf FJ. Biometry. San Francisco: W. H. Freeman and co.; 1981.

Garcia-Del-Rey E, Kleven O, Lifjeld JT. Extrapair paternity in insular African blue tits Cyanistes teneriffae is no less frequent than in continental Eurasian blue tits Cyanistes caeruleus. Ibis. 2012;154(4):862–867. doi: 10.1111/j.1474-919X.2012.01241.x. DOI

Gohli J, Leder EH, Garcia-del-Rey E, Johannessen LE, Johnsen A, Laskemoen T, Popp M, Lifjeld JT. The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs. Mol Ecol. 2015;24(1):180–191. doi: 10.1111/mec.13008. PubMed DOI

Hogner S, Laskemoen T, Lifjeld JT, Pavel V, Chutný B, García J, Eybert M-C, Matsyna E, Johnsen A. Rapid sperm evolution in the bluethroat (Luscinia svecica) subspecies complex. Behav Ecol Sociobiol. 2013;67(8):1205–1217. doi: 10.1007/s00265-013-1548-z. DOI

Schmoll T, Kleven O. Sperm dimensions differ between two coal tit Periparus ater populations. J Ornithol. 2011;152(3):515–520. doi: 10.1007/s10336-010-0603-z. DOI

Johnsen A, Lifjeld JT. Ecological constraints on extra-pair paternity in the bluethroat. Oecologia. 2003;136(3):476–483. doi: 10.1007/s00442-003-1286-4. PubMed DOI

Simmons LW, Moore AJ. Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm Biology: An Evolutionary Perspective. Oxford: Elsevier; 2009. pp. 405–434.

Laskemoen T, Kleven O, Johannessen LE, Fossøy F, Robertson RJ, Lifjeld JT. Repeatability of sperm size and motility within and between seasons in the barn swallow (Hirundo rustica) J Ornithol. 2013;154(4):955–963. doi: 10.1007/s10336-013-0961-4. DOI

Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M. The effects of life history and sexual selection on male and female plumage colouration. Nature. 2015;527(7578):367–370. doi: 10.1038/nature15509. PubMed DOI

Tobias JA, Sheard C, Seddon N, Meade A, Cotton AJ, Nakagawa S. Territoriality, social bonds, and the evolution of communal signaling in birds. Front Ecol Evol. 2016;4:74. doi: 10.3389/fevo.2016.00074. DOI

Rodewald PE. The birds of North America online. In. Cornell Laboratory of Ornithology: Ithaca, New York; 2015.

Albrecht T, Kleven O, Kreisinger J, Laskemoen T, Omotoriogun TC, Ottosson U, Reif J, Sedláček O, Hořák D, Robertson RJ, Lifjeld JT. Sperm competition in tropical versus temperate zone birds. Proc R Soc B. 2013;280(1752):20122434. doi: 10.1098/rspb.2012.2434. PubMed DOI PMC

R Development Core Team. R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna: R Foundation for statistical computing; 2011. http://www.R-project.org.

Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W. caper: Comparative Analyses of Phylogenetics and Evolution in R. Version 0.5.2. 2013.

Pagel M. Inferring evolutionary processes from phylogenies. Zool Scr. 1997;26(4):331–348. doi: 10.1111/j.1463-6409.1997.tb00423.x. DOI

Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res. 2004;33(2):261–304. doi: 10.1177/0049124104268644. DOI

Burnham K, Anderson D, Huyvaert K. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 2011;65(1):23–35. doi: 10.1007/s00265-010-1029-6. DOI

Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2009.

Petrie M, Doums C, Møller AP. The degree of extra-pair paternity increases with genetic variability. Proc Natl Acad Sci U S A. 1998;95(16):9390–9395. doi: 10.1073/pnas.95.16.9390. PubMed DOI PMC

Whittingham LA, Dunn PO. Male parental care and paternity. Curr Ornithol. 2001;16:257–298.

Owens IPF, Bennett PM. Mortality costs of parental care and sexual dimorphism in birds. Proc R Soc B. 1994;257(1348):1–8. doi: 10.1098/rspb.1994.0086. DOI

Mauck RA, Marschall EA, Parker PG. Adult survival and imperfect assessment of parentage: effects on male parenting decisions. Am Nat. 1999;154(1):99–109. doi: 10.1086/303216. PubMed DOI

Westneat DF, Sherman PW. Parentage and the evolution of parental behavior. Behav Ecol. 1993;4(1):66–77. doi: 10.1093/beheco/4.1.66. DOI

Gowaty PA. Battles of the sexes and origins of monogamy. In: Black JM, editor. Partnerships in birds: the study of monogamy. Oxford: Oxford University Press; 1996. pp. 21–52.

Ketterson ED, Nolan VJ. Male parental behavior in birds. Ann Rev Ecol Syst. 1994;25:601–628. doi: 10.1146/annurev.es.25.110194.003125. DOI

Cezilly F, Nager R. Comparative evidence for a positive association between divorce and extra-pair paternity in birds. Proc R Soc B. 1995;262:7–12. doi: 10.1098/rspb.1995.0169. DOI

Møller AP, Birkhead TR. The evolution of plumage brightness in birds is related to extrapair paternity. Evolution. 1994;48(4):1089–1100. doi: 10.1111/j.1558-5646.1994.tb05296.x. PubMed DOI

Owens IPF, Hartley IR. Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc B. 1998;265(1394):397–407. doi: 10.1098/rspb.1998.0308. DOI

Møller AP. Immune defence, extra-pair paternity, and sexual selection in birds. Proc R Soc B. 1997;264(1381):561–566. doi: 10.1098/rspb.1997.0080. DOI

Dunn PO, Whittingham LA, Pitcher TE. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution. 2001;55(1):161–175. doi: 10.1111/j.0014-3820.2001.tb01281.x. PubMed DOI

Westneat DF, Stewart IRK. Extra-pair paternity in birds: causes, correlates and conflict. Ann Rev Ecol Evol Syst. 2003;34(1):365–396. doi: 10.1146/annurev.ecolsys.34.011802.132439. DOI

Pitcher TE, Dunn PO, Whittingham LA. Sperm competition and the evolution of testes size in birds. J Evol Biol. 2005;18(3):557–567. doi: 10.1111/j.1420-9101.2004.00874.x. PubMed DOI

Gohli J, Lifjeld JT, Albrecht T. Migration distance is positively associated with sex-linked genetic diversity in passerine birds. Ethol Ecol Evol. 2015;28(1):42–52. doi: 10.1080/03949370.2015.1018954. DOI

Koprivnikar J, Leung TLF. Flying with diverse passengers: greater richness of parasitic nematodes in migratory birds. Oikos. 2015;124(4):399–405. doi: 10.1111/oik.01799. DOI

Leung TLF, Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol. 2016;85(6):1471–1480. doi: 10.1111/1365-2656.12581. PubMed DOI

Møller AP, Erritzøe J. Host immune defence and migration in birds. Evol Ecol. 1998;12(8):945–953. doi: 10.1023/A:1006516222343. DOI

Gohli J, Anmarkrud JA, Johnsen A, Kleven O, Borge T, Lifjeld JT. Female promiscuity is positively associated with neutral and selected genetic diversity in passerine birds. Evolution. 2013;67(5):1406–1419. PubMed

Lifjeld JT, Gohli J, Johnsen A. Promiscuity, sexual selection, and genetic diversity: a reply to Spurgin. Evolution. 2013;67(10):3073–3074. PubMed

Arct A, Drobniak S, Podmokła E, Gustafson L, Cichoń M. Benefits of extra-pair mating may depend on environmental conditions—an experimental study in the blue tit (Cyanistes caeruleus) Behav Ecol Sociobiol. 2013;67(11):1809–1815. doi: 10.1007/s00265-013-1588-4. PubMed DOI PMC

Fossøy F, Johnsen A, Lifjeld JT. Multiple genetic benefits of female promiscuity in a socially monogamous passerine. Evolution. 2008;62(1):145–156. doi: 10.1111/j.1558-5646.2007.00284.x. PubMed DOI

Johnsen A, Andersen V, Sunding C, Lifjeld JT. Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature. 2000;406(6793):296–299. doi: 10.1038/35018556. PubMed DOI

Garvin JC, Abroe B, Pedersen MC, Dunn PO, Whittingham LA. Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol Ecol. 2006;15(12):3833–3840. doi: 10.1111/j.1365-294X.2006.03042.x. PubMed DOI

Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K. Is there a latitudinal gradient in the importance of biotic interactions? Ann Rev Ecol Evol Syst. 2009;40(1):245–269. doi: 10.1146/annurev.ecolsys.39.110707.173430. DOI

Garamszegi LZ, Eens M, Hurtrez-Bousses S, Moller AP. Testosterone, testes size, and mating success in birds: a comparative study. Horm Behav. 2005;47(4):389–409. doi: 10.1016/j.yhbeh.2004.11.008. PubMed DOI

Møller AP. Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am Nat. 1991;137(6):882–906. doi: 10.1086/285199. DOI

Davies NB, Hatchwell BJ, Robson T, Burke T. Paternity and parental effort in dunnocks Prunella modularis: how good are male chick-feeding rules? Anim Behav. 1992;43(5):729–745. doi: 10.1016/S0003-3472(05)80197-6. DOI

Hartley IR, Davies NB, Hatchwell BJ, Desrochers A, Nebel D, Burke T. The polygynandrous mating system of the alpine accentor, Prunella collaris. II. Multiple paternity and parental effort. Anim Behav. 1995;49(3):789–803. doi: 10.1016/0003-3472(95)80210-X. DOI

Lively CM, Dybdahl MF. Parasite adaptation to locally common host genotypes. Nature. 2000;405(6787):679–681. doi: 10.1038/35015069. PubMed DOI

Morran LT, Schmidt OG, Gelarden IA, Parrish RC, Lively CM. Running with the red queen: host-parasite coevolution selects for biparental sex. Science. 2011;333(6039):216–218. doi: 10.1126/science.1206360. PubMed DOI PMC