Abstract
Skewed adult sex ratio (ASR) has been proposed to be a consequence of breeding individuals producing a biassed primary sex ratio, sexual differences in offspring mortality or juvenile dispersal, or sexual differences in adult mortality. In this study, we analysed if a skewed primary sex ratio, sexual differences in recruitment and/or sexual differences in adult survival were responsible for the sustained male-skewed ASR in a south temperate population of house wrens (Troglodytes aedon bonariae). Molecular sex determination of 229 nestlings raised from 56 nests during two consecutive breeding seasons showed that primary sex ratio did not depart significantly from equality. Also, although females are the dispersing sex, differences in the number of males and females recruited into the population did not explain the skewed ASR. Finally, survival analysis of marked and re-sighted breeding individuals using a 2004–2017 database revealed that males had a significant higher survival probability than females (overall annual survival probability: 0.53 vs. 0.34, respectively), and explained a high amount of variance in the inter-annual ASR variation. As adult individuals showed a high philopatry to their breeding territories both within and amongst breeding seasons and we never found any marked individual of our study site in the neighbouring populations, we suggest that the skewed ASR observed in this population can be mainly attributed to sexual differences in adult survival.
Zusammenfassung
Das Geschlechterverhältnis bei adulten Hauszaunkönigen der südlichen gemäßigten Zone wird durch geschlechtsspezifische Unterschiede in der Überlebenswahrscheinlichkeit der Adulten erklärt
Es wird angenommen, dass ein verschobenes Geschlechterverhältnis bei adulten Individuen (ASR; engl. adult sex ratio) eine Folge eines von brütenden Individuen erzeugten verschobenen primären Geschlechterverhältnisses, von geschlechtsspezifischen Unterschieden in der Sterblichkeit der Nachkommen oder in der räumlichen Ausbreitung von Juvenilen oder in der Sterblichkeit der Adulten ist. In dieser Studie analysierten wir, inwiefern ein verschobenes primäres Geschlechterverhältnis, geschlechtsspezifische Unterschiede bei der Rekrutierung und/oder beim Überleben der Adulten für das anhaltende zu Männchen verschobene ASR in einer Population des Hauszaunkönigs Troglodytes aedon bonariae der südlichen gemäßigten Zone verantwortlich ist. Die molekulare Geschlechterbestimmung von 229 Nestlingen aus 56 Nestern in zwei aufeinanderfolgenden Brutsaisons zeigte, dass das primäre Geschlechterverhältnis nicht signifikant von einem ausgewogenen Verhältnis abweicht. Darüber hinaus erklärten die Unterschiede in der Anzahl der in die Population rekrutierten Männchen und Weibchen nicht das verschobene ASR, auch wenn die Weibchen das sich ausbreitende Geschlecht darstellen. Schließlich ergaben Überlebensanalysen (engl. survival analysis) von markierten und wieder gesichteten brütenden Individuen unter Verwendung einer Datenbank aus den Jahren 2004 bis 2017, dass Männchen eine signifikant höhere Überlebenswahrscheinlichkeit als Weibchen haben (jährliche Gesamtüberlebenswahrscheinlichkeit: 0,53 vs. 0,34), und dies erklärte einen hohen Anteil der Varianz der zwischenjährlichen ASR-Variationen. Da adulte Individuen sowohl innerhalb der Brutsaison als auch zwischen Brutsaisons eine hohe Brutortstreue zeigten und wir in den Nachbarpopulationen nie ein markiertes Individuum aus unserem Untersuchungsgebiet gefunden haben, gehen wir davon aus, dass das in dieser Population beobachtete verschobene ASR hauptsächlich auf geschlechtsspezifische Unterschiede im Überleben der Adulten zurückzuführen ist.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Albrecht DJ, Johnson LS (2002) Manipulation of offspring sex ratio by second-mated female house wrens. Proc R Soc B 269:461–465. https://doi.org/10.1098/rspb.2001.1914
Ancona S, Liker A, Carmona-Isunza MC, Székely T (2020) Sex differences in age-to-maturation relate to sexual selection and adult sex ratios in birds. Evol Lett 4:44–53. https://doi.org/10.1002/evl3.156
Arroyo BE (2002) Fledgling sex ratio variation and future reproduction probability in Montagu’s harrier, Circus pygargus. Behav Ecol Sociobiol 52:109–116. https://doi.org/10.1007/s00265-002-0496-9
Barbosa AM, Real R, Munoz AR, Brown JA (2013) New measures for assessing model equilibrium and prediction mismatch in species distribution models. Divers Distrib 19:1333–1338. https://doi.org/10.1111/ddi.12100
Barrett EL, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921. https://doi.org/10.1111/j.1474-9726.2011.00741.x
Breitwisch R (1989) Mortality patterns, sex ratios, and parental investment in monogamous birds. Curr Ornithol 6:1–50
Brewer D (2001) Wrens, dippers and thrashers. Yale Univ Press, New Haven
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400. https://doi.org/10.3929/ethz-b-000240890
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Cain KE, Hall ML, Medina I, Leitao AV, Delhey K, Brouwer L, Peters A, Pruett-Jones S, Webster MS, Langmore NE, Mulder RA (2019) Conspicuous plumage does not increase predation risk: a continent-wide test using model songbirds. Am Nat 193:359–372. https://doi.org/10.1086/701632
Carro ME, Fernández GJ (2023) Density-dependent natal philopatry in southern House Wrens. Ibis 165:436–447. https://doi.org/10.1111/ibi.13157
Carro ME, Mermoz ME, Fernández GJ (2014) Factors affecting the probability of double brooding by Southern House Wrens. J Field Ornithol 85:227–236. https://doi.org/10.1111/jofo.12064
Carro ME, Llambías PE, Fernández GJ (2017) Mate and territory availability affect breeding dispersal and divorce in a resident Southern House Wren Troglodytes aedon musculus population. Ibis 159:168–179. https://doi.org/10.1111/ibi.12438
Carro ME, Llambías PE, Mahler B, Fernández GJ (2021) Contrasting patterns of natal dispersal of a south temperate house wren population at local and regional scales. J Ornithol 162:895–907. https://doi.org/10.1007/s10336-021-01887-9
Clout MN, Elliott GP, Robertson BC (2002) Effects of supplementary feeding on the offspring sex ratio of Kakapo: a dilemma for the conservation of a polygynous parrot. Biol Conserv 107:13–18. https://doi.org/10.1016/S0006-3207(01)00267-1
Clutton-Brock TH (1986) Sex ratio variation in birds. Ibis 128:317–329. https://doi.org/10.1111/j.1474-919X.1986.tb02682.x
Donald PF (2007) Adult sex ratios in wild bird populations. Ibis 149:671–692. https://doi.org/10.1111/j.1474-919X.2007.00724.x
Dubois NS, Dale Kennedy E, Getty T (2006) Surplus nest boxes and the potential for polygyny affect clutch size and offspring sex ratio in house wrens. Proc R Soc B 273:1751–1757. https://doi.org/10.1098/rspb.2006.3509
Eberhart-Phillips LJ, Küpper C, Miller TE, Cruz-López M, Maher KH, Dos Remedios N, Stoffel MA, Hoffman JI, Krüger O, Székely T (2017) Sex-specific early survival drives adult sex ratio bias in snowy plovers and impacts mating system and population growth. Proc Natl Acad Sci 114:E5474–E5481. https://doi.org/10.1073/pnas.1620043114
Ewen JG, Clarke RH, Moysey E, Boulton RL, Crozier RH, Clarke MF (2001) Primary sex ratio bias in an endangered cooperatively breeding bird, the black-eared miner, and its implications for conservation. Biol Conserv 101:137–145. https://doi.org/10.1016/S0006-3207(01)00022-2
Fernández GJ, Carro ME (2021) Effects of nest predation on a south temperate house wren population. J Avian Biol 52:e02632. https://doi.org/10.1111/jav.02632
Fernández GJ, Carro ME, Llambias PE (2020) Spatial and temporal variation in breeding parameters of two south-temperate populations of House Wrens. J Field Ornithol 91:13–30. https://doi.org/10.1111/jofo.12319
Fisher RA (1930) The genetical theory of natural selection. Oxford Univ Press, London
Freed LA (1987) The long-term pair bond of tropical house wrens: advantage or constraint? Am Nat 130:507–525. https://doi.org/10.1086/284728
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. https://doi.org/10.1016/s0003-3472(80)80103-5
Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Ann Rev Ecol Syst 13:1–21. https://doi.org/10.1146/annurev.es.13.110182.000245
Griffin AS, Sheldon BC, West SA (2005) Cooperative breeders adjust offspring sex ratios to produce helpful helpers. Am Nat 166:628–632. https://doi.org/10.1086/491662
Griffiths R, Daan S, Dijkstra C (1996) Sex identification in birds using two CHD genes. Proc Roy Soc B 263:1251–1256. https://doi.org/10.1098/rspb.1996.0184
Gustafsson L (1990) Life-history trade-offs and optimal clutch size in relation to age in the Collared Flycatcher. In: Blondel J, Gosler A, Lebreton JD, McCleery R (eds) Population biology of passerine birds. NATO ASI Series, vol 24. Springer, Berlin, pp 235–245
Hartig F (2020) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package ver. 0.3.3.0. http://florianhartig.github.io/DHARMa/. Accessed 25 June 2021
Heinsohn R, Olah G, Webb M, Peakall R, Stojanovic D (2018) Sex ratio bias and shared paternity reduce individual fitness and population viability in a critically endangered parrot. J Anim Ecol 88:502–510. https://doi.org/10.1111/1365-2656.12922
Huhta E, Rytkönen S, Solonen T (2003) Plumage brightness of prey increases predation risk: an among species comparison. Ecology 84:1793–1799. https://doi.org/10.1890/0012-9658(2003)084[1793:PBOPIP]2.0.CO;2
Jaatinen K, Lehikoinen A, Lank DB (2010) Female-biased sex ratios and the proportion of cryptic male morphs of migrant juvenile ruffs (Philomachus pugnax) in Finland. Ornis Fenn 87:125–134
Janota SM, Soukup SS, Thompson CF (2002) Male-biased offspring sex ratio in the house wren. Condor 104:881–885. https://doi.org/10.1093/condor/104.4.881
Johnson LS (2014) House wren Troglodytes aedon. In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology and American Ornithologists’ Union
Johnson LS, Kermott LH (1990) Possible causes of territory takeovers in a north-temperate population of house wrens. Auk 107:781–784. https://doi.org/10.2307/4088013
Kalmbach E, Benito MM (2007) Sexual size dimorphism and offspring vulnerability in birds. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles. Oxford Univ. Press, Oxford, pp 133–142
Kokko H, Jennions MD (2008) Parental investment, sexual selection and sex ratios. J Evol Biol 21:919–948. https://doi.org/10.1111/j.1420-9101.2008.01540.x
Komdeur J (1996) Facultative sex ratio bias in the offspring of Seychelles warblers. Proc R Soc B 263:661–666. https://doi.org/10.1098/rspb.1996.0099
Komdeur J, Székely T, Long X, Kingma SA (2017) Adult sex ratios and their implications for cooperative breeding in birds. Phil Trans R Soc B 372:20160322. https://doi.org/10.1098/rstb.2016.0322
Kosztolányi A, Barta Z, Küpper C, Szekely T (2011) Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird. J Evol Biol 24:1842–1846. https://doi.org/10.1111/j.1420-9101.2011.02305.x
Lehikoinen A, Öst M, Hollmén T, Kilpi M (2008) Does sex-specific duckling mortality contribute to male bias in adult common eiders. Condor 110:574–578. https://doi.org/10.1525/cond.2008.8574
Ligon JD (1999) The evolution of avian breeding systems. Oxford Univ. Press, Oxford
Liker A, Székely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897. https://doi.org/10.1554/04-560
Liker A, Freckleton RP, Székely T (2013) The evolution of sex roles in birds is related to adult sex ratio. Nat Commun 4:1587. https://doi.org/10.1038/ncomms2600
Lima SL (2009) Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev 84:485–513. https://doi.org/10.1111/j.1469-185x.2009.00085.x
Llambías PE (2012) How do Southern House Wrens Troglodytes aedon musculus achieve polygyny? An experimental approach. J Ornithol 153:571–578. https://doi.org/10.1007/s10336-011-0778-y
Llambías PE, Fernández GJ (2009) Effects of nest boxes on the breeding biology of House Wrens in the southern temperate zone. Ibis 151:113–121. https://doi.org/10.1111/j.1474-919x.2008.00868.x
Llambías PE, LaBarbera K, Astié AA (2012) Similar patterns of parental provisioning in a monogamous and a polygynous population of the house wren. Condor 114:629–638. https://doi.org/10.1525/cond.2012.110066
Llambías PE, Carro ME, Fernández GJ (2015) Latitudinal differences in life-history traits and parental care in northern and southern temperate zone House Wrens. J Ornithol 156:933–942. https://doi.org/10.1007/s10336-015-1217-2
Loonstra AJ, Verhoeven MA, Senner NR, Hooijmeijer JC, Piersma T, Kentie R (2019) Natal habitat and sex-specific survival rates result in a male-biased adult sex ratio. Behav Ecol 30:843–851. https://doi.org/10.1093/beheco/arz021
Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D (2021) Performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6:3139. https://doi.org/10.21105/joss.03139
Martín CA, Alonso JC, Alonso JA, Palacín C, Magana M, Martín B (2007) Sex-biased juvenile survival in a bird with extreme size dimorphism, the great bustard Otis tarda. J Avian Biol 38:335–346. https://doi.org/10.1111/j.2007.0908-8857.03811.x
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215. https://doi.org/10.1093/nar/16.3.1215
Møller AP, Nielsen JT, Garamszegi LZ (2006) Song post exposure, song features, and predation risk. Behav Ecol 17:155–163. https://doi.org/10.1093/beheco/arj010
Morrison CA, Robinson RA, Clark JA, Gill JA (2016) Causes and consequences of spatial variation in sex ratios in a declining bird species. J Anim Ecol 85:1298–1306. https://doi.org/10.1111/1365-2656.12556
Nager RG, Monaghan P, Houston DC, Genovart M (2000) Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behav Ecol Sociobiol 48:452–457. https://doi.org/10.1007/s002650000262
Post P, Götmark F (2006) Foraging behavior and predation risk in male and female Eurasian Blackbirds (Turdus merula) during the breeding season. Auk 123:162–170. https://doi.org/10.1093/auk/123.1.162
Promislow DE, Montgomerie R, Martin TE (1992) Mortality costs of sexual dimorphism in birds. Proc Royal Soc B 250:143–150. https://doi.org/10.1098/rspb.1992.0142
Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299. https://doi.org/10.1016/0169-5347(87)90081-4
Ralph CJ, Geupel GR, Pyle P, Martin TE, DeSante DF (1993) Handbookof field methods for monitoring landbirds. Gen. Tech. Rep. PSW-GTR-144-www. Albany, Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, CA, p 41
Reid WV (1987) The cost of reproduction in the glaucous-winged gull. Oecologia 74:458–467. https://doi.org/10.1007/bf00378945
Sargeant AB, Allen SH, Eberhardt RT (1984) Red fox predation on breeding ducks in midcontinent North America. Wildl Monog 89:3–41
Smith JNM, Yom-Tov Y, Moses R (1982) Polygyny, male parental care, and sex ratio in Song Sparrows: an experimental study. Auk 99:555–564. https://doi.org/10.1093/auk/99.3.555
Steifetten Ø, Dale S (2006) Viability of an endangered population of ortolan buntings: the effect of a skewed operational sex ratio. Biol Conserv 132:88–97. https://doi.org/10.1016/j.biocon.2006.03.016
Stutchbury BJ, Hill JR III, Kramer PM, Rush SA, Tarof SA (2009) Sex and age-specific annual survival in a Neotropical migratory songbird, the Purple Martin (Prognes ubis). Auk 126:278–287. https://doi.org/10.1525/auk.2009.08038
Székely T, Weissing FJ, Komdeur J (2014a) Adult sex ratio variation: Implications for breeding system evolution. J Evol Biol 27:1500–1512. https://doi.org/10.1111/jeb.12415
Székely T, Liker A, Freckleton RP, Fichtel C, Kappeler PM (2014b) Sex-biased survival predicts adult sex ratio variation in wild birds. Proc R Soc B 281:20140342. https://doi.org/10.1098/rspb.2014.0342
Teather KL, Weatherhead PJ (1989) Sex-specific mortality in nestling great-tailed grackles. Ecology 70:1485–1493. https://doi.org/10.2307/1938207
Thomson DL, Monaghan PAT, Furness RW (1998) The demands of incubation and avian clutch size. Biol Rev 73:293–304. https://doi.org/10.1111/j.1469-185x.1998.tb00032.x
Tuero DT, Fiorini VD, Reboreda JC (2007) Effects of Shiny Cowbird Molothrus bonariensis parasitism on different components of House Wren Troglodytes aedon reproductive success. Ibis 149:521–529. https://doi.org/10.1111/j.1474-919X.2007.00676.x
Van Oosten HH, Schekkerman H (2021) Female-biased adult sex ratio in relation to sex-specific adult and first-year survival, fledgling sex ratio and dispersal in a migratory passerine. Ardea 109:55–65. https://doi.org/10.5253/arde.v109i1.a8
Vervoorst FB (1967) Las comunidades vegetales de la Depresión del Salado (Provincia de Buenos Aires). INTA, Buenos Aires, Argentina
Ward MP, Schlossberg S (2004) Conspecific attraction and the conservation of territorial songbirds. Conserv Biol 18:519–525. https://doi.org/10.1111/j.1523-1739.2004.00494.x
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(sup1):S120–S139
Acknowledgements
We thank Luis García and his wife Anahí for allowing us to work on his ranch in Buenos Aires, and Martha Busai, Mario Beade and families for logistical support. We also thank two anonymous reviewers for their constructive comments and suggestions on an earlier version of the manuscript. This work was supported by the University of Buenos Aires (UBACyT 20020090200117), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PIP112-200901-00011) grants to GJF and the E. Alexander Bergstrom Research Awards programme of the Association of Field Ornithologists 2010 to MEC. All methods used in the present study meet the ethical requirements for science research and comply with the current laws of the country in which they were performed. This study and the protocols we used were approved by the Organización Provincial para el Desarrollo Sustentable (OPDS) from the Buenos Aires province, Argentina (Disp. 019/15).
Author contributions
MEC and GJF designed the study and collected the field data. MEC and GJF did the statistical analysis. BM and MEC carried out the molecular analyses in the laboratory. All authors contributed to the writing of the paper and approved its final stage.
Funding
This work was supported by the University of Buenos Aires (UBACyT 20020090200117), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PIP112-200901-00011) Grants to GJF and the E. Alexander Bergstrom Research Awards programme of the Association of Field Ornithologists 2010 to MEC.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interest.
Ethical approval
All methods used in the present study meet the ethical requirements for science research and comply with the current laws of the country in which they were performed. This study and the protocols we used were approved by the Organización Provincial para el Desarrollo Sustentable (OPDS) from the Buenos Aires province, Argentina (Disp. 019/15).
Additional information
Communicated by S. Bouwhuis.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
Carro, M.E., Fernández, G.J. & Mahler, B. Adult sex ratio in south temperate house wrens is explained by sexual differences in adult survival. J Ornithol 165, 115–125 (2024). https://doi.org/10.1007/s10336-023-02088-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-023-02088-2