in

It is hard to be small: Inbreeding depression on male breeding success depends on body size in a threatened songbird


Abstract

While inbreeding is known to affect individual fitness and thus population extinction risk, studies often under-represent non-model species of conservation concern and rarely examine the conditionality of inbreeding depression. Here, using genomic markers (SNPs), we determined inbreeding depression in a threatened bird, the aquatic warbler Acrocephalus paludicola – a habitat specialist with depleted genetic diversity that went through a steep recent decline. We also explored whether the magnitude of inbreeding depression depends on phenotypic (tarsus and wing length) and environmental (timing of breeding and brood size) factors. In adult males, the relationship between genomic inbreeding and breeding success depended on tarsus length, a proxy for body size, being strongly negative in small-tarsus males. We also detected a weak interaction effect between genomic inbreeding and wing length on male survival, with short-winged males being negatively affected by inbreeding. By contrast, models that did not include these interactions provided little evidence for inbreeding effects on male fitness, and estimates of inbreeding load were highly uncertain for both survival and breeding success. In adult females, we found little support for associations between genomic inbreeding and clutch size, hatching success, nestling survival, or fledged brood size, and no evidence that these relationships were conditional on the phenotypic and environmental variables examined. Accordingly, estimates of inbreeding load in females were close to zero. We conclude that inbreeding depression on fitness components is phenotype-dependent, being stronger in small-bodied males, and that considering interactions with phenotypic variables enables more accurate estimation of inbreeding depression.

Access through your institution

Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Map of the study area.
The alternative text for this image may have been generated using AI.
Fig. 2: Inbreeding depression on fitness components in male adult aquatic warblers.
The alternative text for this image may have been generated using AI.

Similar content being viewed by others

Little evidence of inbreeding depression for birth mass, survival and growth in Antarctic fur seal pups

Parasite-mediated inbreeding depression in wild red deer

Inbreeding depression explains killer whale population dynamics

Data availability

Raw sequencing data and metadata are available in the Sequence Read Archive (Bioproject PRJNA1155693). The Python scripts used in the R2SCOs pipeline are available at https://git.imp.fu-berlin.de/begendiv/stacks2r2scos, and those used to process the population libraries can be found at https://git.imp.fu-berlin.de/begendiv/radseq-preprocessing-pipeline/-/tree/main/scripts. Individual genotype data, datasets, and R code used for the analysis can be downloaded from https://data.mendeley.com/datasets/z3fhnkjsd3.

References

  • Andrews KR, Adams JR, Cassirer EF, Plowright RK, Gardner C, Dwire M et al. (2018) A bioinformatic pipeline for identifying informative SNP panels for parentage assignment from RADseq data. Mol Ecol Resour 18:1263–1281.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242.

    Article 
    CAS 
    PubMed 

    Google Scholar 

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

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.

    Article 

    Google Scholar 

  • Bayona-Vásquez NJ, Glenn TC, Kieran TJ, Pierson TW, Hoffberg SL, Scott PA et al. (2019) Adapterama III: Quadruple-indexed, double/triple-enzyme RADseq libraries (2RAD/3RAD). PeerJ 7: e7724.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Beccardi M, Pen I, Bichet C, Tschirren B, Vedder O (2024) Inbreeding accelerates reproductive senescence, but not survival senescence, in a precocial bird. J Anim Ecol 93:1972–1982.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bellebaum J (2018) Population dynamics. In: Tanneberger F, Kubacka J (eds) The Aquatic Warbler conservation handbook, Brandenburg State Office for Environment (LfU): Potsdam, Germany, pp 68–71.

  • Border JA, Atkinson LR, Henderson IG, Hartley IR (2018) Nest monitoring does not affect nesting success of Whinchats Saxicola rubetra. Ibis 160:624–633.

    Article 

    Google Scholar 

  • Briedis M, Keišs O (2016) Extracting historical population trends using archival ringing data – an example: the globally threatened Aquatic Warbler. J Ornithol 157:419–425.

    Article 

    Google Scholar 

  • Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Ecol Soc 6:16.

    Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al. (2017) {glmmTMB} Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling. R J 9:378–400.

    Article 

    Google Scholar 

  • Brown CR, Brown MB (2003) Testis size increases with colony size in cliff swallows. Behav Ecol 14:569–575.

    Article 

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach, 2nd edn. Springer-Verlag: New York, USA.

  • Caravaggi A, Sam B, Richard JF, Iván de la H, Mike PS, Smith JA (2021) The long and short of it: converting between maximum and minimum tarsus measurements in passerine birds. Ringing Migr 36:9–17.

    Article 

    Google Scholar 

  • Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: Building and genotyping loci de novo from short-read sequences. G3 Genes|Genomes|Genetics 1:171–182.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: An analysis tool set for population genomics. Mol Ecol 22:3124–3140.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cleasby IR, Burke T, Schroeder J, Nakagawa S (2011) Food supplements increase adult tarsus length, but not growth rate, in an island population of house sparrows (Passer domesticus). BMC Res Notes 4: 431.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270.

    Article 
    PubMed 

    Google Scholar 

  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al. (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 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.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Deerenberg C, de Kogel CH, Overkamp GFJ (1996) Costs of reproduction in the Zebra Finch Taeniopygia guttata: manipulation of brood size in the laboratory. J Avian Biol 27:321–326.

    Article 

    Google Scholar 

  • Driller M, Arantes LS, Vilaça ST, Carrasco-Valenzuela T, Heeger F, Mbedi S, et al. (2021). Achieving high-quality ddRAD-like reference catalogs for non-model species: the power of overlapping paired-end reads. bioRxiv: 2020.04.03.024331.

  • Duntsch L, Whibley A, de Villemereuil P, Brekke P, Bailey S, Ewen JG et al. (2023) Genomic signatures of inbreeding depression for a threatened Aotearoa New Zealand passerine. Mol Ecol 32:1893–1907.

    Article 
    PubMed 

    Google Scholar 

  • Dyrcz A, Wink M, Backhaus A, Zdunek W, Leisler B, Schulze-Hagen K (2002) Correlates of multiple paternity in the Aquatic Warbler (Acrocephalus paludicola). J Ornithol 143:430–439.

    Google Scholar 

  • Dyrcz A, Wink M, Kruszewicz A, Leisler B (2005) Male reproductive success is correlated with blood parasite levels and body condition in the promiscuous Aquatic Warbler (Acrocephalus paludicola). Auk 122:558–565.

    Article 

    Google Scholar 

  • Dyrcz A, Zdunek W (1993) Breeding ecology of the Aquatic Warbler Acrocephalus paludicola on the Biebrza marshes, northeast Poland. Ibis 135:181–189.

    Article 

    Google Scholar 

  • Enders LS, Nunney L (2012) Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster. Proc R Soc B Biol Sci 279:3756–3764.

    Article 

    Google Scholar 

  • Faux P, Oliveira JCP, Campos DP, Dantas GPM, Maia TA, Dergan CG et al. (2020) Fast genomic analysis of aquatic bird populations from short single-end reads considering sex-related pitfalls. Ecol Inform 56:101058.

    Article 

    Google Scholar 

  • Flade M, Malashevich U, Krogulec J, Poluda A, Preiksa Z, Végvári Z, et al. (2018). World distribution, population, and trends. In: Tanneberger F, Kubacka J (eds) The Aquatic Warbler conservation handbook, Brandenburg State Office for Environment (LfU): Potsdam, Germany, pp 22–35.

  • Forstmeier W, Ihle M, Opatová P, Martin K, Knief U, Albrechtová J et al. (2017) Testing the phenotype-linked fertility hypothesis in the presence and absence of inbreeding. J Evol Biol 30:968–976.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258.

    Article 
    PubMed 

    Google Scholar 

  • Gage MJG, Surridge AK, Tomkins JL, Green E, Wiskin L, Bell DJ et al. (2006) Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr Biol 16:612–617.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Garamszegi LZ (2011) Information-theoretic approaches to statistical analysis in behavioural ecology: an introduction. Behav Ecol Sociobiol 65:1–11.

    Article 

    Google Scholar 

  • Gebhardt-Henrich S, Richner H (1998). Causes of growth variation and its consequences for fitness. In: Starck JM, Ricklefs RE (eds) Avian Growth and Development, Oxford University Press: New York, NY, USA, pp 324–339.

  • Girndt A, Cockburn G, Sánchez-Tójar A, Hertel M, Burke T, Schroeder J (2019) Male age and its association with reproductive traits in captive and wild house sparrows. J Evol Biol 32:1432–1443.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez NJ, Finger JW et al. (2019) Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ 7: e7755.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gruber B, Unmack PJ, Berry OF, Georges A (2018) dartR: An R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Mol Ecol Resour 18:691–699.

    Article 
    PubMed 

    Google Scholar 

  • Grueber CE, Laws RJ, Nakagawa S, Jamieson IG (2010) Inbreeding depression accumulation across life-history stages of the endangered takahe. Conserv Biol 24:1617–1625.

    Article 
    PubMed 

    Google Scholar 

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hahn S, Korner-Nievergelt F, Emmenegger T, Amrhein V, Csörgő T, Gursoy A et al. (2016) Longer wings for faster springs – wing length relates to spring phenology in a long-distance migrant across its range. Ecol Evol 6:68–77.

    Article 
    PubMed 

    Google Scholar 

  • Harrell FE (2015) Multivariable modeling strategies. In: Harrell Frank E. J (ed) Regression Modeling Strategies: With Applications to Linear Models, Logistic and Ordinal Regression, and Survival Analysis, Springer International Publishing: Cham, pp 63–102.

  • Harrisson KA, Magrath MJL, Yen JDL, Pavlova A, Murray N, Quin B et al. (2019) Lifetime fitness costs of inbreeding and being inbred in a critically endangered bird. Curr Biol 29:2711–2717.e4.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hayward A, Gillooly JF (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS One 6:e16557.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hemmings NL, Slate J, Birkhead TR (2012a) Inbreeding causes early death in a passerine bird. Nat Commun 3: 863.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hemmings N, West M, Birkhead TR (2012b) Causes of hatching failure in endangered birds. Biol Lett 8:964–967.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hinkson KM, Poo S (2020) Inbreeding depression in sperm quality in a critically endangered amphibian. Zoo Biol 39:197–204.

    Article 
    PubMed 

    Google Scholar 

  • Huisman J, Kruuk LEB, Ellis PA, Clutton-Brock T, Pemberton JM (2016) Inbreeding depression across the lifespan in a wild mammal population. Proc Natl Acad Sci 113:3585–3590.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • IPCC (2023). Summary for policymakers. In: Core Writing Team, Lee H, Romero J (eds) Climate Change 2023: Synthesis report. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC: Geneva, Switzerland, pp 1–34.

  • Jamieson IG, Roy MS, Lettink M (2003) Sex-specific consequences of recent inbreeding in an ancestrally inbred population of New Zealand Takahe. Conserv Biol 17:708–716.

    Article 

    Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555.

    Article 
    PubMed 

    Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106.

    Article 
    PubMed 

    Google Scholar 

  • Kardos M, Luikart G, Allendorf FW (2015) Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees. Heredity 115:63–72.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

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

    PubMed 

    Google Scholar 

  • Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin’s finches. Evolution 56:1229–1239.

    Article 
    PubMed 

    Google Scholar 

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

    Article 

    Google Scholar 

  • Kennedy ES, Grueber CE, Duncan RP, Jamieson IG (2014) Severe inbreeding depression and no evidence of purging in an extremely inbred wild species—the Chatham Island Black Robin. Evolution 68:987–995.

    Article 
    PubMed 

    Google Scholar 

  • De Kogel CH (1997) Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. J Anim Ecol 66:167–178.

    Article 

    Google Scholar 

  • Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proceedings Biol Sci 269:1581–1589.

    Article 

    Google Scholar 

  • Kubacka J, Dubiec A, Korb J, Salewski V, Dyrcz A, Foucher J et al. (2024) Low genetic diversity and high gene flow in the Aquatic Warbler (Acrocephalus paludicola), a threatened marshland songbird with a fragmented breeding range. Ibis 166:232–251.

    Article 

    Google Scholar 

  • Kubacka J, Dubiec A, Souza Arantes L, Herdegen-Radwan M, Mazzoni CJ, Sparmann S et al. (2025) Agonistic song rate positively correlates with male breeding success and avian malaria infection in Acrocephalus paludicola (Aquatic Warbler), a promiscuous songbird with female-only parental care. Ornithology 142:ukae045.

    Article 

    Google Scholar 

  • Kubacka J, Oppel S, Dyrcz A, Lachmann L, Barros Da Costa JPD, Kail U et al. (2014) Effect of mowing on productivity in the endangered Aquatic Warbler Acrocephalus paludicola. Bird Conserv Int 24:45–58.

    Article 

    Google Scholar 

  • Kyriazis CC, Wayne RK, Lohmueller KE (2021) Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression. Evol Lett 5:33–47.

    Article 
    PubMed 

    Google Scholar 

  • Laws RJ, Townsend SM, Nakagawa S, Jamieson IG (2010) Limited inbreeding depression in a bottlenecked population is age but not environment dependent. J Avian Biol 41:645–652.

    Article 

    Google Scholar 

  • Leisler B, Schulze-Hagen K (2011) Reed warblers reproduced. In: The Reed Warblers. Diversity in a uniform family, KNNV Publishing: Zeist, the Netherlands, pp 138–159.

  • Marr AB, Arcese P, Hochachka WM, Reid JM, Keller LF (2006) Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J Anim Ecol 75:1406–1415.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mattey SN, Strutt L, Smiseth PT (2013) Intergenerational effects of inbreeding in Nicrophorus vespilloides: offspring suffer fitness costs when either they or their parents are inbred. J Evol Biol 26:843–853.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Matthews TJ, HE Cottee-Jones, Whittaker RJ (2014) Habitat fragmentation and the species–area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Divers Distrib 20:1136–1146.

    Article 

    Google Scholar 

  • Mazerolle MJ (2023) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c).

  • McGillycuddy M, Warton DI, Popovic G, Bolker BM (2025) Parsimoniously fitting large multivariate random effects in {glmmTMB}. J Stat Softw 112:1–19.

    Article 

    Google Scholar 

  • Merom K, McCleery R, Yom-Tov Y (1999) Age-related changes in wing-length and body mass in the Reed Warbler Acrocephalus scirpaceus and Clamorous Reed Warbler A. stentoreus. Bird Study 46:249–255.

    Article 

    Google Scholar 

  • Morton NE, Crow JF (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proc Natl Acad Sci USA 42:855–863.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Le Nevé A, Blaize C, Dehorter O, Dugué H, Hemery D, Jiguet F, et al. (2018) Migration. In: Tanneberger F, Kubacka J (eds) The Aquatic Warbler conservation handbook, Brandenburg State Office for Environment (LfU): Potsdam, Germany, pp 72–89.

  • Nietlisbach P, Muff S, Reid JM, Whitlock MC, Keller LF (2019) Nonequivalent lethal equivalents: Models and inbreeding metrics for unbiased estimation of inbreeding load. Evol Appl 12:266–279.

    Article 
    PubMed 

    Google Scholar 

  • Niskanen AK, Billing AM, Holand H, Hagen IJ, Araya-Ajoy YG, Husby A et al. (2020) Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation. Proc Natl Acad Sci 117:14584–14592.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nonaka E, Sirén J, Somervuo P, Ruokolainen L, Ovaskainen O, Hanski I (2019) Scaling up the effects of inbreeding depression from individuals to metapopulations. J Anim Ecol 88:1202–1214.

    Article 
    PubMed 

    Google Scholar 

  • Noordwijk AJ, Van, Scharloo W (1981) Inbreeding in an island population of the Great Tit. Evolution 35:674–688.

    Article 
    PubMed 

    Google Scholar 

  • O’Grady JJ, Brook BW, Reed DH, Ballou JD, Tonkyn DW, Frankham R (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol Conserv 133:42–51.

    Article 

    Google Scholar 

  • Ożarowska A, Zaniewicz G, Meissner W (2021) Sex and age-specific differences in wing pointedness and wing length in blackcaps Sylvia atricapilla migrating through the southern Baltic coast. Curr Zool 67:271–277.

    Article 
    PubMed 

    Google Scholar 

  • Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934.

    Article 
    PubMed 

    Google Scholar 

  • Pemberton JM, Ellis PE, Pilkington JG, Bérénos C (2017) Inbreeding depression by environment interactions in a free-living mammal population. Heredity 118:64–77.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Pflüger FJ, Signer J, Balkenhol N (2019) Habitat loss causes non-linear genetic erosion in specialist species. Glob Ecol Conserv 17:e00507.

    Google Scholar 

  • Płóciennik JBC, Hałupka L (2025) The effect of research activities on nest predation in the Eurasian Reed Warbler Acrocephalus scirpaceus. Eur Zool J 92:382–389.

    Article 

    Google Scholar 

  • Pooley EL, Kennedy MW, Nager RG (2014) Maternal inbreeding reduces parental care in the zebra finch, Taeniopygia guttata. Anim Behav 97:153–163.

    Article 

    Google Scholar 

  • R Core Team (2025). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

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

    Article 

    Google Scholar 

  • Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89.

    Article 

    Google Scholar 

  • Risely A, Nightingale J, Richardson DS, Barr I (2013) Wing length and age, but not tarsus or mass, independently determine spring arrival at breeding territories in a long-distance migrant the Common Whitethroat, Sylvia communis. Bird Study 60:539–546.

    Article 

    Google Scholar 

  • Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674.

    Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113.

    Article 

    Google Scholar 

  • Schulze-Hagen K, Swatschek I, Dyrcz A, Wink M (1993) Multiple Vaterschaften in Bruten des Seggenrohrsängers Acrocephalus paludicola: Erste Ergebnisse des DNA-Fingerprintings. J Ornithol 134:145–154.

    Article 

    Google Scholar 

  • Searcy WA, Peters S, Nowicki S (2004) Effects of early nutrition on growth rate and adult size in song sparrows Melospiza melodia. J Avian Biol 35:269–279.

    Article 

    Google Scholar 

  • Senar JC, Pascual J (1997) Keel and tarsus length may provide a good predictor of avian body size. Ardea 85.

  • Sin SYW, Hoover BA, Nevitt GA, Edwards SV (2021) Demographic history, not mating system, explains signatures of inbreeding and inbreeding depression in a large outbred population. Am Nat 197:658–676.

    Article 
    PubMed 

    Google Scholar 

  • Smith HG, Källander H, Nilsson J-Å (1989) The trade-off between offspring number and quality in the Great Tit Parus major. J Anim Ecol 58:383–401.

    Article 

    Google Scholar 

  • Stewart IF (1963) Variation of wing length with age. Bird Study 10:1–9.

    Article 

    Google Scholar 

  • Stoffel MA, Esser M, Kardos M, Humble E, Nichols H, David P et al. (2016) inbreedR: an R package for the analysis of inbreeding based on genetic markers. Methods Ecol Evol 7:1331–1339.

    Article 

    Google Scholar 

  • Stoffel MA, Johnston SE, Pilkington JG, Pemberton JM (2021) Genetic architecture and lifetime dynamics of inbreeding depression in a wild mammal. Nat Commun 12: 2972.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Stolt B-O, Fransson T (1995) Body mass, wing length and spring arrival of the Ortolan Bunting Emberiza hortulana. Ornis Fenn 72:14–18.

    Google Scholar 

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21.

    Article 

    Google Scholar 

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

    PubMed 

    Google Scholar 

  • Szulkin M, Garant D, McCleery RH, Sheldon BC (2007) Inbreeding depression along a life-history continuum in the great tit. J Evol Biol 20:1531–1543.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Szulkin M, Sheldon BC (2007) The environmental dependence of inbreeding depression in a wild bird population. PLoS One 2: e1027.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tanneberger F, Kloskowski J, Knöfler V, Kozulin A, Marczakiewicz P, Morkvėnas Ž, et al. (2018a). Breeding habitat requirements. In: Tanneberger F, Kubacka J (eds) The Aquatic Warbler conservation handbook, Brandenburg State Office for Environment (LfU): Potsdam, Germany, pp 34–45.

  • Tanneberger F, Kozulin A, Poluda A, Bellebaum J, Lachmann L, Flade M (2018b). Threats and limiting factors. In: Tanneberger F, Kubacka J (eds) The Aquatic Warbler conservation handbook, Brandenburg State Office for Environment (LfU): Potsdam, Germany, pp 106–121.

  • Tarof SA, Kramer PM, Tautin J, Stutchbury BJM (2012) Effects of known age on male paternity in a migratory songbird. Behav Ecol 23:313–321.

    Article 

    Google Scholar 

  • Thrasher DJ, Butcher BG, Campagna L, Webster MS, Lovette IJ (2018) Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: A proof of concept in a highly promiscuous bird. Mol Ecol Resour 18:953–965.

    Article 
    CAS 

    Google Scholar 

  • Verhulst S, Nilsson JÅ (2008) The timing of birds’ breeding seasons: A review of experiments that manipulated timing of breeding. Philos Trans R Soc B Biol Sci 363:399–410.

    Article 

    Google Scholar 

  • Wang J (2022) A joint likelihood estimator of relatedness and allele frequencies from a small sample of individuals. Methods Ecol Evol 13:2443–2462.

    Article 

    Google Scholar 

  • Wang J (2025) EMIBD9: Estimating 9 condensed IBD coefficients, inbreeding and relatedness from marker genotypes. Heredity 134:155–161.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Weidinger K (2008) Nest monitoring does not increase nest predation in open-nesting songbirds: inference from continuous nest-survival data. Auk 125:859–868.

    Article 

    Google Scholar 

  • Westemeier RL, Brawn JD, Simpson SA, Esker TL, Jansen RW, Walk JW et al. (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York

  • Wolak ME, Arcese P, Keller LF, Nietlisbach P, Reid JM (2018) Sex-specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding. Evolution 72:2057–2075.

    Article 
    PubMed 

    Google Scholar 

  • Wołoszkiewicz J, Kubacka J, Kloskowski J (2024) Breeding ecology of the globally threatened Aquatic Warbler Acrocephalus paludicola in calcareous fens at the south-western range limit. Bird Conserv Int 34:e40.

    Article 

    Google Scholar 

  • Zuur AF, Ieno EN (2021) The World of Zero-Inflated Models. 1: Using GLM. Highland Statistics Ltd.: Newburgh, United Kingdom.

Download references

Acknowledgements

Grzegorz Kiljan, Pedro Costa, Piotr Guzik, Marta Celej, Julien Foucher, Beata Głębocka, Aneta Gołębiewska, Maciej Kamiński, Agnieszka Kuczyńska, Romuald Mikusek, Łukasz Mucha, Felix Närmann, Edyta Podmokła, Aneta Rybińska, Paulina Siejka, Michał Walesiak, and Laura Zani assisted in the field. Alina Gerlée kindly prepared the map. Gugny Field Station of the University of Białystok provided accommodation and workspace during fieldwork. Susan Mbedi, Ismael Reyes, and Katarzyna Dudek supported the preparation and sequencing of RAD libraries, and Wiesław Babik provided lab space and equipment. The lab work and bioinformatic analysis were partially funded by the German Federal Ministry of Education and Research (BMBF, Förderkennzeichen 033W034A). The sequencing was performed in cooperation with the Competence Center for Genome Analysis at the Christian-Albrechts-University in Kiel and at the Berlin Center for Genomics in Biodiversity Research. We thank Przemysław Chylarecki, who provided advice on the statistical analysis. The study was funded by the Polish National Science Centre’s grant no. 2016/20/S/NZ8/00434. We thank the editor and three anonymous referees for comments on previous versions of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

JK designed and performed research; SS, JK & MHR carried out lab work; LSA, MHR, CJM & JK performed bioinformatic analysis; JK conducted statistical and parentage analysis; JK, TO & CJM provided funding and resources; JK wrote the paper; all the authors edited drafts.

Corresponding author

Correspondence to
Justyna Kubacka.

Ethics declarations

Competing interests

The authors declare no competing interests.

Research Ethics

The study was aligned with the Polish animal welfare and conservation law. Bird capture was conducted under permits from the Polish Ministry of Environment (DOP-WPN.286.38.2016.AN, DOP-WPN.286.40.2016.AN) and the Regional Directorate of Environmental Protection in Białystok (WPN.6401.244.2016.MN). Ringing was performed by licensed ringers. Blood samples were collected under a permit from the I Local Ethical Committee in Warsaw (185/2016).

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Armando Caballero.

Supplementary information

Supplementary Material (download PDF )

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Cite this article

Kubacka, J., Arantes, L.S., Herdegen-Radwan, M. et al. It is hard to be small: Inbreeding depression on male breeding success depends on body size in a threatened songbird.
Heredity (2026). https://doi.org/10.1038/s41437-026-00859-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Version of record:

  • DOI: https://doi.org/10.1038/s41437-026-00859-0


Source: Ecology - nature.com

Impact of land use change on the long-term economic value of carbon sequestration in Central Alborz, Iran

Humidity as a potential zeitgeber for circadian entrainment of insect systems