Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Published Online January 31, 2002
Science DOI: 10.1126/science.1069043

Research Articles

Submitted on December 17, 2001
Accepted on January 24, 2002

Constraints in the Evolution of Sex Ratio Adjustment

Stuart A. West 1* Ben C. Sheldon 2

1 Institute of Cell, Animal, and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, UK.
2 Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK.

* To whom correspondence should be addressed. E-mail: stu.west{at}ed.ac.uk.

When the relative fitness of male and female offspring varies with environmental conditions, evolutionary theory predicts that parents should adjust the sex of their offspring accordingly. Qualitative, and even quantitative, support for this prediction is striking in some taxa, but much less convincing in others. Explaining such variation across taxa in the fit of sex ratio theory remains a major challenge. We use meta-analysis to test the role of two constraints in the evolution of sex ratios. Based on analysis of sex ratio skews in birds and wasps we show that: (1) mechanisms of sex determination do not necessarily constrain the evolution of sex ratio adjustment, and (2) parental ability to predict their offspring's environment influences the evolution of sex ratio patterns across taxa. More generally, our results show that multiple constraints may determine the precision of adaptation.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs.
N. Saino, M. Romano, M. Caprioli, R. Ambrosini, D. Rubolini, and M. Fasola (2009)
Proc R Soc B
   Abstract »    Full Text »    PDF »
How does breeding system variation modulate sexual antagonism?.
S. Bedhomme, G. Bernasconi, J. M. Koene, A. Lankinen, H. S. Arathi, N. K. Michiels, and N. Anthes (2009)
Biol Lett 5, 717-720
   Abstract »    Full Text »    PDF »
Sex allocation conflict in insect societies: who wins?.
H. Helantera and F. L. W. Ratnieks (2009)
Biol Lett 5, 700-704
   Abstract »    Full Text »    PDF »
Extra-pair young in house wren broods are more likely to be male than female.
L. S. Johnson, C. F. Thompson, S. K. Sakaluk, M. Neuhauser, B. G.P. Johnson, S. S. Soukup, S. J. Forsythe, and B. S. Masters (2009)
Proc R Soc B 276, 2285-2289
   Abstract »    Full Text »    PDF »
Maternal effects in cooperative breeders: from hymenopterans to humans.
A. F Russell and V. Lummaa (2009)
Phil Trans R Soc B 364, 1143-1167
   Abstract »    Full Text »    PDF »
Genetic Incompatibility Drives Sex Allocation and Maternal Investment in a Polymorphic Finch.
S. R. Pryke and S. C. Griffith (2009)
Science 323, 1605-1607
   Abstract »    Full Text »    PDF »
Sex allocation in response to local resource competition over breeding territories.
M. B. Hjernquist, K. A. Thuman Hjernquist, J. T. Forsman, and L. Gustafsson (2009)
Behav. Ecol. 20, 335-339
   Abstract »    Full Text »    PDF »
The mechanism of sex ratio adjustment in a pollinating fig wasp.
S. Raja, N. Suleman, S. G Compton, and J. C Moore (2008)
Proc R Soc B 275, 1603-1610
   Abstract »    Full Text »    PDF »
Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds.
J. Rutkowska and A. V Badyaev (2008)
Phil Trans R Soc B 363, 1675-1686
   Abstract »    Full Text »    PDF »
Split sex ratios in the social Hymenoptera: a meta-analysis.
J. Meunier, S. A. West, and M. Chapuisat (2008)
Behav. Ecol. 19, 382-390
   Abstract »    Full Text »    PDF »
Strong but variable associations between social dominance and clutch sex ratio in a colonial corvid.
H.M. Salomons, C. Dijkstra, and S. Verhulst (2008)
Behav. Ecol. 19, 417-424
   Abstract »    Full Text »    PDF »
Temperature-related birth sex ratio bias in historical Sami: warm years bring more sons.
S. Helle, S. Helama, and J. Jokela (2008)
Biol Lett 4, 60-62
   Abstract »    Full Text »    PDF »
Male twins reduce fitness of female co-twins in humans.
V. Lummaa, J. E. Pettay, and A. F. Russell (2007)
PNAS 104, 10915-10920
   Abstract »    Full Text »    PDF »
The 'big spenders' of the steppe: sex-specific maternal allocation and twinning in the saiga antelope.
A. Kuhl, A. Mysterud, G. I Erdnenov, A. A Lushchekina, I. A Grachev, A. B Bekenov, and E.J Milner-Gulland (2007)
Proc R Soc B 274, 1293-1299
   Abstract »    Full Text »    PDF »
Male phenotypic quality influences offspring sex ratio in a polygynous ungulate.
K. H Roed, O. Holand, A. Mysterud, A. Tverdal, J. Kumpula, and M. Nieminen (2007)
Proc R Soc B 274, 727-733
   Abstract »    Full Text »    PDF »
Fertilization success and UV ornamentation in blue tits Cyanistes caeruleus: correlational and experimental evidence.
K. Delhey, A. Peters, A. Johnsen, and B. Kempenaers (2007)
Behav. Ecol. 18, 399-409
   Abstract »    Full Text »    PDF »
Litter size and fetal sex ratio adjustment in a highly polytocous species: the wild boar.
S. Servanty, J.-M. Gaillard, D. Allaine, S. Brandt, and E. Baubet (2007)
Behav. Ecol. 18, 427-432
   Abstract »    Full Text »    PDF »
Reproducing lizards modify sex allocation in response to operational sex ratios.
D. A Warner and R. Shine (2007)
Biol Lett 3, 47-50
   Abstract »    Full Text »    PDF »
Should attractive males have more sons?.
T. W. Fawcett, B. Kuijper, I. Pen, and F. J. Weissing (2007)
Behav. Ecol. 18, 71-80
   Abstract »    Full Text »    PDF »
Nuclear Sex-Determining Genes Cause Large Sex-Ratio Variation in the Apple Snail Pomacea canaliculata.
Y. Yusa (2007)
Genetics 175, 179-184
   Abstract »    Full Text »    PDF »
Consistent sex ratio bias of individual female dragon lizards.
T. Uller, B. Mott, G. Odierna, and M. Olsson (2006)
Biol Lett 2, 569-572
   Abstract »    Full Text »    PDF »
Revised evidence for facultative sex ratio adjustment in birds: a correction.
P. Cassey, J. G Ewen, and A. P Moller (2006)
Proc R Soc B 273, 3129-3130
   Abstract »    Full Text »    PDF »
Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird.
A. V. Badyaev, T. L. Hamstra, K. P. Oh, and D. A. Acevedo Seaman (2006)
PNAS 103, 14406-14411
   Abstract »    Full Text »    PDF »
Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits.
P. Korsten, C. M. Lessells, A. C. Mateman, M. van der Velde, and J. Komdeur (2006)
Behav. Ecol. 17, 539-546
   Abstract »    Full Text »    PDF »
Sex allocation theory aids species conservation.
B. C Robertson, G. P Elliott, D. K Eason, M. N Clout, and N. J Gemmell (2006)
Biol Lett 2, 229-231
   Abstract »    Full Text »    PDF »
Sex ratios under asymmetrical local mate competition in the parasitoid wasp Nasonia vitripennis.
D. M. Shuker, I. Pen, and S. A. West (2006)
Behav. Ecol. 17, 345-352
   Abstract »    Full Text »    PDF »
Offspring sex ratio allocation in the parasitic jaeger: selection for pale females and melanic males?.
K. Janssen, K. E. Erikstad, and S. Bensch (2006)
Behav. Ecol. 17, 236-245
   Abstract »    Full Text »    PDF »
Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters.
N. Saino, R. P. Ferrari, M. Romano, R. Martinelli, A. Lacroix, D. Gil, and A. P. Moller (2006)
Behav. Ecol. 17, 172-181
   Abstract »    Full Text »    PDF »
How outcrossing hermaphrodites sense the presence of conspecifics and suppress female allocation.
D. Schleicherova, M. C. Lorenzi, and G. Sella (2006)
Behav. Ecol. 17, 1-5
   Abstract »    Full Text »    PDF »
Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird.
A. V Badyaev, H. Schwabl, R. L Young, R. A Duckworth, K. J Navara, and A.F Parlow (2005)
Proc R Soc B 272, 2165-2172
   Abstract »    Full Text »    PDF »
No sex difference in yolk steroid concentrations of avian eggs at laying.
K. M Pilz, E. Adkins-Regan, and H. Schwabl (2005)
Biol Lett 1, 318-321
   Abstract »    Full Text »    PDF »
Differential sex allocation in sand lizards: bright males induce daughter production in a species with heteromorphic sex chromosomes.
M. Olsson, E. Wapstra, and T. Uller (2005)
Biol Lett 1, 378-380
   Abstract »    Full Text »    PDF »
Maternal influences on brood sex ratios: an experimental study in tree swallows.
L. A Whittingham, P. O Dunn, and J. K Nooker (2005)
Proc R Soc B 272, 1775-1780
   Abstract »    Full Text »    PDF »
Sex allocation in response to paternal attractiveness in the zebra finch.
A.N. Rutstein, H.E. Gorman, K.E. Arnold, L. Gilbert, K.J. Orr, A. Adam, R. Nager, and J.A. Graves (2005)
Behav. Ecol. 16, 763-769
   Abstract »    Full Text »    PDF »
Sex ratio strategies and the evolution of cue use.
J. C Moore, M. Zavodna, S. G Compton, and P. M Gilmartin (2005)
Proc R Soc B 272, 1287-1294
   Abstract »    Full Text »    PDF »
Maternal rank and local resource competition do not predict birth sex ratios in wild baboons.
J. B Silk, E. Willoughby, and G. R Brown (2005)
Proc R Soc B 272, 859-864
   Abstract »    Full Text »    PDF »
Host cell preference and variable transmission strategies in malaria parasites.
S. E Reece, A. B Duncan, S. A West, and A. F Read (2005)
Proc R Soc B 272, 511-517
   Abstract »    Full Text »    PDF »
Offspring sex ratios correlate with pair-male condition in a cooperatively breeding fairy-wren.
M. K. Rathburn and R. Montgomerie (2005)
Behav. Ecol. 16, 41-47
   Abstract »    Full Text »    PDF »
Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota.
D. Allaine (2004)
Behav. Ecol. 15, 997-1002
   Abstract »    Full Text »    PDF »
Maternal Diet and Other Factors Affecting Offspring Sex Ratio: A Review.
C. S. Rosenfeld and R. M. Roberts (2004)
Biol Reprod 71, 1063-1070
   Abstract »    Full Text »    PDF »
Birth sex ratio and social rank: consistency and variability within and between primate groups.
G. Schino (2004)
Behav. Ecol. 15, 850-856
   Abstract »    Full Text »    PDF »
Information constraints and the precision of adaptation: Sex ratio manipulation in wasps.
D. M. Shuker and S. A. West (2004)
PNAS 101, 10363-10367
   Abstract »    Full Text »    PDF »
Against the odds? Nestling sex ratio variation in green-rumped parrotlets.
A. E. Budden and S. R. Beissinger (2004)
Behav. Ecol. 15, 607-613
   Abstract »    Full Text »    PDF »
Sex allocation within broods: the intrabrood sharing-out hypothesis.
J. Carranza (2004)
Behav. Ecol. 15, 223-232
   Abstract »    Full Text »    PDF »
Brood sex ratio in the Kentish plover.
T. Szekely, I. C. Cuthill, S. Yezerinac, R. Griffiths, and J. Kis (2004)
Behav. Ecol. 15, 58-62
   Abstract »    Full Text »    PDF »
Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment.
T. L. F. Martins (2004)
Behav. Ecol. 15, 174-180
   Abstract »    Full Text »    PDF »
Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate.
C. S. Rosenfeld, K. M. Grimm, K. A. Livingston, A. M. Brokman, W. E. Lamberson, and R. M. Roberts (2003)
PNAS 100, 4628-4632
   Abstract »    Full Text »    PDF »
Facultative control of offspring sex in the cooperatively breeding bell miner, Manorina melanophrys.
J. G. Ewen, R. H. Crozier, P. Cassey, T. Ward-Smith, J. N. Painter, R. J. Robertson, D. A. Jones, and M. F. Clarke (2003)
Behav. Ecol. 14, 157-164
   Abstract »    Full Text »    PDF »
Reconsidering the null hypothesis: Is maternal rank associated with birth sex ratios in primate groups?.
G. R. Brown and J. B. Silk (2002)
PNAS 99, 11252-11255
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)