Abstract
When fitness returns or production costs vary between male and female offspring, selection is expected to favor females that adjust offspring sex ratio accordingly. However, to what extent vertebrates can do so is the subject of ongoing debate. Here, we explore primary sex ratios in 125 broods of cooperatively breeding purple-crowned fairy-wrens Malurus coronatus. We expected that females might adjust offspring sex ratio because this passerine species experiences considerable variation in social and environmental conditions. (1) However, although helpers substantially increase parental fitness, females (particularly in pairs and small groups) did not overproduce philopatric males (helper-repayment hypothesis). (2) Sex-ratio adjustment based on competition among individuals (helper-competition hypothesis) did not conceal helper-repayment effects or drive sex allocation on its own: while high-quality territories can accommodate more birds, brood sex ratios were independent of territory quality, alone or in interaction with group size. (3) Additionally, males are larger than females and are possibly more costly to produce (costly sex hypothesis), and (4) female offspring may benefit more from long-term effects of favorable conditions early in life (Trivers–Willard hypothesis). Nonetheless, large seasonal variation in food abundance was not associated with a consistent skew in primary sex ratios. Thus, overall, our results did not support the main hypotheses of adaptive sex-ratio adjustment in M. coronatus. We discuss that long-term differential costs and benefits may be insufficient to drive evolution of primary sex-ratio manipulation by M. coronatus females. More investigation is therefore needed to determine the general required sex differences in long-term fitness returns for mechanisms of primary sex-ratio manipulation to evolve.
Similar content being viewed by others
References
Andersson DJ, Reeve J, Martinez Gomez JE, Weathers WW, Hutson S, Cunningham HV, Bird DM (1993) Sexual size dimorphism and food requirements of nestling birds. Can J Zool 71:2541–2545
Appleby BM, Petty SJ, Blakey JK, Rainey P, Macdonald DW (1997) Does variation of sex-ratio enhance reproductive success of offspring in the tawny owl (Strix aluco)? Proc R Soc Lond B 264:1111–1116
Bates D, Sarkar D (2007) Lme4: linear mixed-effects models using S4 Classes. R package version 0.9975-12. Available at: http://CRAN.R-project.org/
Bradbury RB, Cutton PA, Wright J, Griffiths R (1997) Nestling sex-ratio in the European starling Sturnus vulgaris. J Avian Biol 28:255–258
Byholm P, Brommer JE, Saurola P (2002) Scale and seasonal sex-ratio trends in northern goshawk Accipiter gentilis broods. J Avian Biol 33:399–406
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton
Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 208:1157–1159
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
Clutton-Brock T (1986) Sex ratio variation in birds. Ibis 128:317–329
Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Ann Rev Ecolog Syst 29:141–177
Cockburn A, Double MC (2008) Cooperatively breeding superb fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits. Behav Ecol Sociobiol 62:681–688
Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals: can the hypotheses be disentangled? In: Hardy ICW (ed) Sex ratios. Concepts and research methods. Cambridge University Press, Cambridge, pp 266–286
Cordero PJ, Griffith SC, Aparico JM, Parkin DT (2000) Sexual dimorphism in house sparrow eggs. Behav Ecol Sociobiol 48:353–357
Dijkstra C, Daan S, Meijer T, Cavé AJ, Foppen R (1988) Body mass of the kestrel in relation to food abundance and reproduction. Ardea 76:127–140
Dijkstra C, Daan S, Buker JB (1990) Adaptive seasonal variation in the sex ratio of kestrel broods. Funct Ecol 4:143–147
Emlen ST (1997) When mothers prefer daughters over sons. Trends Ecol Evol 12:291–292
Emlen ST, Emlen JM, Levin S (1986) Sex-ratio in species with helpers-at-the-nest. Am Nat 127:1–8
Ewen JG, Cassey P, Møller AP (2004) Facultative primary sex ratio variation: a lack of evidence in birds? Proc R Soc Lond B 271:1277–1282
Fiala KL, Congdon JD (1983) Energetic consequences of sexual size dimorphism in nestling red-winged blackbirds. Ecology 64:642–647
Fisher RA (1930) The genetic theory of natural selection, 2nd edn. Clarendon, Oxford
Frank SA (1990) Sex allocation theory for birds and mammals. Annu Rev Ecol Syst 21:13–55
Gowaty PA, Lennartz MR (1985) Sex ratios of nestling and fledgling red-cockaded woodpeckers (Picoides borealis) favor males. Am Nat 16:347–353
Griffin AS, Sheldon BC, West SA (2005) Cooperative breeders adjust offspring sex ratios to produce helpful helpers. Am Nat 166:628–632
Hall ML, Peters A (2008) Coordination between the sexes for territorial defence in a duetting fairy-wren. Anim Behav 76:65–73
Hall ML, Peters A (2009) Do male paternity guards ensure female fidelity in a duetting fairy-wren? Behav Ecol 20:222–228
Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488
Hatchwell BJ (1999) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil Trans R Soc B 364:3217–3227
Hauber ME, Lacey EA (2005) Bateman’s principle in cooperatively breeding vertebrates: the effect of non-breeding alloparents on variability in female and male reproductive success. Integr Comp Biol 45:903–914
Howe HF (1977) Sex-ratio adjustment in the common grackle. Science 198:744–746
Julliard R (2000) Sex-specific dispersal in spatially varying environments leads to habitat-dependent evolutionary stable sex ratio. Behav Ecol 4:421–428
Kahn MZ, Walters JR (2002) Effects of helpers on breeder survival in the red-cockaded woodpecker (Picoides borealis). Behav Ecol Sociobiol 51:336–344
Kahn NW, St John J, Quinn TW (1998) Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds. Auk 115:1074–1078
Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56:155–164
Kingma SA, Hall ML, Segelbacher G, Peters A (2009) Radical loss of an extreme extra-pair mating system. BMC Ecol 9:15
Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79:757–768
Koenig WD, Walters JR (1999) Sex-ratio selection in species with helpers at the nest: the repayment model revisited. Am Nat 153:124–130
Komdeur J (2004) Sex-ratio manipulation. In: Koenig WD, Dickinson JL (eds) Ecology and behaviour of booperative breeding in birds. Cambridge University Press, Cambridge, pp 102–116
Komdeur J, Pen I (2002) Adaptive sex allocation in birds. Philos Trans R Soc Lond B 357:373–386
Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385:522–525
Korpimäki E, May CA, Parkin DT, Wetton JH, Wiehn J (2000) Environmental- and parental condition-related variation in sex ratio of kestrel broods. J Avian Biol 31:128–134
Krackow S (1999) Avian sex ratio distortions: the myth of maternal control. In: Adams NJ, Slotow RH (eds) Proc. 22 Int. Ornithol. Congr. Durban. Johannesburg, BirdLife South Africa, pp 425–433
Legge S, Heinsohn R, Double MC, Griffiths R, Cockburn A (2001) Complex sex allocation in the laughing kookaburra. Behav Ecol 12:524–533
Leimar O (1996) Life-history analysis of the Trivers and Willard sex ratio problem. Behav Ecol 7:316–325
Lessells CM, Avery MI (1987) Sex ratio selection in species with helpers at the nest: some extensions of the repayment model. Am Nat 129:610–620
Ligon JD, Ligon SH (1990) Female-biased sex ratio at hatching in the green woodhoopoe. Auk 107:765–771
Nager RG, Managhan P, Griffiths R, Houston DC, Dawson R (1999) Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci USA 96:570–573
Olsen PD, Cockburn A (1991) Female-biased sex allocation in peregrine falcons and other raptors. Behav Ecol Sociobiol 28:417–423
Patterson CB, Erckmann WJ, Orians GH (1980) An experimental study of parental investment and polygyny in male blackbirds. Am Nat 116:757–769
Pen I, Weissing FJ (2000) Sex ratio optimization with helpers at the nest. Proc R Soc Lond B 267:539–544
Pike TW (2005) Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection. Behav Ecol Sociobiol 58:407–413
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer, New York
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team R-Core (2009) Nlme: linear and nonlinear mixed effects models. R-package version 3:1–94
R Development Core Team. 2010. R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. Available at: http://www.r-project.org.
Rathburn MK, Montgomerie R (2005) Offspring sex ratios correlate with pair-male condition in a cooperatively breeding fairy-wren. Behav Ecol 16:41–47
Richardson D, Jury F, Blaakmeer K, Komdeur J, Burke T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10:2263–2273
Rösner D, Bogatz K, Trapp H, Grünkorn T, Brandl R (2009) No evidence of skewed secondary sex ratios in nestling of the Common Raven (Corvus corax). J Orn 150:293–297
Rowley I, Russell E (1993) The purple-crowned fairy-wren Malurus coronatus. 2. breeding biology, social organisation, demography and management. Emu 93:235–250
Rowley I, Russell E (1997) Fairy-wrens and grasswrens. Oxford University Press, Oxford
Rubenstein DR (2007) Temporal but not spatial environmental variation drives adaptive offspring sex allocation in a plural cooperative breeder. Am Nat 170:155–165
Rubenstein DR, Lovette IJ (2009) Reproductive skew and selection on female ornamentation in social species. Nature 462:786–789
Seger J, Stubblefield JW (2002) Models of sex ratio evolution. In: Hardy ICW (ed) Sex ratios. Concepts and research methods. Cambridge University Press, Cambridge, pp 2–25
Sheldon BC, Andersson S, Griffith SC, Örnborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877
Shine R, Brown GP (2008) Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics. Phil Trans R Soc B 363:363–373
Sunde P, Bolstad MS, Møller JD (2003) Reversed sexual dimorphism in Tawny Owls, Strix aluco, correlates with duty division in breeding effort. Oikos 101:265–278
Thuman KA, Widemo F, Griffith SC (2003) Condition-dependent sex allocation in a lek-breeding wader, the ruff (Philomachus pugnax). Mol Ecol 12:213–218
Torres R, Drummond H (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68:1133–1141
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92
Varian-Ramos CW, Karubian J, Talbott V, Tapia I, Webster MS (2010) Offspring sex ratios reflect lack of repayment by auxiliary males in a cooperatively breeding passerine. Behav Ecol Sociobiol 64:967–977
West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688
West SA, Reece SE, Sheldon BC (2002) Sex ratios. Heredity 88:117–124
West SA, Shuker DM, Sheldon BC (2005) Sex-ratio adjustment when relatives interact: a test of constraints on adaptation. Evolution 59:1211–1228
Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree-swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129
Wiebe KL, Bortolotti GR (1992) Facultative sex ratio manipulation in American kestrels. Behav Ecol Sociobiol 30:379–386
Williams GC (1979) The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B 205:567–580
Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy ICW (ed) Sex ratios. Concepts and research methods. Cambridge University Press, Cambridge, pp 48–92
Acknowledgments
We are extremely grateful to Sarah Legge, Steve Murphy, and other staff at the Mornington Wildlife Sanctuary, to the Australian Wildlife Conservancy for logistical support, and to our team of field assistants for their hard work in the field. We thank Evi Fricke for molecular sexing, Joanne Heathcote for collecting rainfall data, Kaspar Delhey for discussion, and Charles R. Brown and two anonymous reviewers for comments. All fieldwork was performed with permission from the Max Planck Institute for Ornithology Animal Ethics Committee, the Australian Wildlife Conservancy, the Western Australia Department of Conservation and Land Management (licenses BB002178 and BB002311), and the Australian Bird and Bat Banding Scheme (Authority 2230 and 2073). The research was funded by the “Minerva Sonderprogramm zur Förderung hervorragender Wissenschaftlerinnen” of the Max Planck Society (to AP).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Brown
Rights and permissions
About this article
Cite this article
Kingma, S.A., Hall, M.L. & Peters, A. No evidence for offspring sex-ratio adjustment to social or environmental conditions in cooperatively breeding purple-crowned fairy-wrens. Behav Ecol Sociobiol 65, 1203–1213 (2011). https://doi.org/10.1007/s00265-010-1133-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-010-1133-7