Sexual Dimorphism in Egg Size and Implications Regarding Facultative Manipulation of Sex in Mountain White-Crowned Sparrows

The Condor 89:798-803 0 The CooperOrnithological Society 1987

SEXUAL DIMORPHISM IN EGG SIZE AND IMPLICATIONS REGARDING FACULTATIVE MANIPULATION OF SEX IN MOUNTAIN WHITE-CROWNED SPARROWS

PAUL S. MEAD,~ MARTIN L. MORTON,~ AND BRIAN E. FISH Department of Biology, OccidentalCollege, Los Angeles,CA 90041

Abstract. The volume of male eggsin Mountain White-crowned Sparrows(Zonotrichiu leucophrysoriantha) was slightly larger than that of female eggsin every year of a 5-year study. The volume difference was highly significant(P < 0.01) when data for all years were combined. Male nestlingsalso grew faster than female siblings.Natural history observations on adults suggestthat reproductive successis more variable in male than in female White- crowned Sparrows.Taken together, these data are consistentwith facultative manipulation of offspring sex as proposed under the Trivers and Willard hypothesis (1973). In avian speciesit may be necessarywhen testingthis hypothesisto considerthe relationshipbetween sexand parental investment for individual offspringrather than focusingsolely on differences between broods. Key words: White-crownedSparrow; Zonotrichia leucophrys; egg size;facultative manipulation;parental investment;sex control;sexual dimorphism.

INTRODUCTION ing the sex of their offspring according to their Charles Darwin (187 1) was openly perplexed by ability to invest. For example, in a specieswhere the tendency of some speciesto produce broods a single dominant male will inseminate several of almost exclusively one sex. Since his time it females, mothers able to produce particularly ro- has been discovered that a number of animals bust offspring will have more of their genespres- not only control the sex of their offspring but do ent in the subsequentgeneration if they produce so in a manner likely to increase their overall sons.Conversely, thoseproducing lessrobust off- reproductive fitness (Clutton-Brock 1982). This spring will benefit most by producing females ability for “facultative manipulation”of off- since daughters need not compete to the same spring sex is best known among invertebrates degree for mates. where it is selectedfor by intense local mate com- Because of the way it was originally stated, petition as well as other factors (Hamilton 1967, previous tests of the Trivers-Willard hypothesis Werren 1980, Charnovet al. 1981, Herre 1985). have generally focused on sex ratios in broods Trivers and Willard (1973) have proposed con- produced by females under varying environ- ditions under which selection will favor facul- mental circumstances(Trivers and Willard 1973, tative manipulation among vertebrates, yet sup- Clutton-Brock 1982). Unfortunately, suchan ap- port for their hypothesis has remained elusive proach is likely to be insensitive. Female “con- (Myers 1978, Williams 1979, Clutton-Brock dition” may be difficult to define and enormous 1982, Harmsen and Cooke 1983). sample sizes are required before valid conclu- The Trivers-Willard hypothesisis basedon the sions can be derived from sex ratio data (Wil- assumption that parental investment influences liams 1979, Harmsen and Cooke 1983). More offspring quality and ultimate reproductive suc- importantly, this approach minimizes the differ- cess.It further assumesthat reproductive success encesin quality which may exist between siblings varies more for offspring of one sex than the from the same brood. In avian speciesoffspring other. When these conditions are met, parents quality can vary widely within clutchesas a func- may increase their reproductive fitness by alter- tion of both egg size and hatching times (Ken- deigh 1941; Gibb 1950; Lack 1954; Kendeigh et al. 1956; Ricklefs 1965; Klomp 1970; Parsons I Received 9 November 1986. Final acceptance15 1970, 1975; O’Connor 1975; Pinkowski 1975; April 1987. z Present address: Dartmouth-Hitchcock Medical Howe 1976; Ryden 1978; Ojanen et al. 1981; Center, Hanover, NH 03756. Zach 1982). Thus, while Trivers and Willard 3To whom reprint requestsshould be sent. stated their hypothesis in terms of sex ratios of

17981 SEXUAL DIMORPHISM IN EGG SIZE 799 entire broods, in avian species their argument marked with indelible ink according to laying may be more appropriately evaluated by relating order. Measurements of egg length and breadth sex to parental investment for individual off- were made to the nearest 0.0 1 mm with calipers spring. at various times during the incubation period Of the many forms of avian parental invest- and their volumes calculated accordingto Hoyt’s ment, eggsize is one that is both easily quantified (1979) formula. Egg weight was not measured and well known to influence offspring quality. because of its tendency to vary over the course Egg size has been correlated with hatchling size, of incubation (Ar and Rahn 1980, Carey 1986). nestling growth rates, and nestling survival in a To determine the relative size of eggswithin the variety of species(Parsons 1970, 1975; Nisbett clutch, egg volumes were standardized by sub- 1973; Schifferli 1973; O’Connor 1975; Howe tracting the mean volume of the clutch from the 1976; Nolan and Thompson 1978; Pinkowski volume of each eggand dividing the sum by the 1979; Bancroft 1984). In turn, egg size is influ- standard error in volume for that clutch. Nests enced by a number of genetic and environmental were visited frequently during hatching, allowing factors and commonly varies both within and chicks to be identified according to the specific between clutches(Kendeigh 194 1; Klomp 1970; eggfrom which they hatched. The yield in terms Howe 1976; Ryden 1978; Ojanen et al. 1979, of determining which chick emerged from which 1981; Zach 1982). egg was increased during the last 2 years of the Although White-crowned Sparrows (Zono- study by applying a longitudinally-oriented piece trichia leucophys) are principally monogamous of thread around each egg with small amounts (DeWolfe 1968), there are several lines of evi- of glue. This helped restrain chicks within their dence to suggestthat reproductive successvaries respectiveeggs during the interval between visits more for males than for females. We have doc- (see Mayoh and Zach 1985). Hatchlings were umented several casesof polygyny as indicated toenail-clipped and later banded to assureiden- by adult males that were feeding nestlings at two tity. Data on chicks for whom eggidentity could nests simultaneously, and we have often iden- not be absolutely determined were not used. tified “floater” (unmated) males but not females Nestlings were weighed to the nearest 0.1 g at in our study population (Morton, unpubl. data). 1 and 8 days of age using a triple beam balance. Males also have a lower recruitment rate to the The sex of each nestling was determined just breeding population and longer maximum life prior to fledging by laparotomy and direct visu- spans,suggesting that on average breeding males alization of the gonads. may outlive their mates to breed with another Because Z. 1. oriantha chicks are often fed female (Baptista and Morton 1982; Morton, un- within a few minutes of hatching, it is difficult publ. data). Finally, cuckoldry appears to be to evaluate the relationship between eggvolume common in this population (Sherman and Mor- and hatchling size in the field. For this reason, ton, unpubl. data) and should selectively increase eggswere collectedfrom a conspecificpopulation the variance in male reproductive success(Triv- (Z. 1. nuttalli) breeding near Lompoc, California, ers 1978). Under these circumstances,the Triv- measured as above, and hatched in the labora- ers-Willard hypothesispredicts that females pro- tory. Chicks from these eggswere weighed to the ducing better than average offspring will skew nearest 0.01 g on a Mettler balance within 30 the sexratio of their brood toward males (Trivers min of hatching. and Willard 1973). Extending this reasoning to individual eggs,we predict that larger eggsshould RESULTS AND DISCUSSION become males and smaller eggsfemales. A comparison of egg volumes shows that male eggs were significantly larger than female eggs METHODS both between (one-tailed t = 2.44, P < 0.01) and This study was conducted over a 5-year period within clutches (one-tailed t = 2.08, P < 0.02; in meadowsnear Tioga Pass,Mono County, Cal- Fig. 1). Mean egg volume was larger for males ifornia. Adult Mountain White-crowned Spar- in each of the 5 years of our study. This difference rows (Z. 1. oriantha) were routinely trapped and was statisticallysignificant when data for all years banded with both U.S. Fish and Wildlife Service were combined but not when comparisons were bands and color bands. During the egg-laying limited to individual years (Table 1). There were period, nests were visited daily and the eggs no significant year-to-year differencesin overall 800 P. S. MEAD, M. L. MORTON AND B. E. FISH

TABLE 2. Mean body weights(g) of 17 matched pairs of male-female White-crowned Sparrow siblings at 2 and 8 days of age. 3.10- - 0,3

Age Males FeIIldeS (days) Meall SD Meall SD P - 0.2 3.8 1.00 3.8 0.98 >0.05 II n if : 21.5 1.35 20.4 1.10

O, ’ 5 >

is - 0.0 W TI Egg volume has been correlated with hatchling 0 rtl size and subsequent growth in a number of al- - -0.1 P tricial species (Parsons 1970, 1975; Nisbett 1973; 0 :: 5 Schifferli 1973; O’Connor 1975; Howe 1976; - -0.2 ci Nolan and Thompson 1978; Bancroft 1984). This was shown also in our data. There was a strong positive correlation between egg volume and 2.95 - -0,J hatchling weight in 10 laboratory-hatched Z. 1. nuttalli (r2 = 0.90, P < 0.01). i 1 1 To assessrelative growth rates of male and FIGURE 1. Mean absolute (between clutches) and female nestlings at Tioga Pass, we selected 17 standardizedvolumes (within clutches)of male (squares) pairs of male and female siblings who, because and female (circles)Mountain White-crowned Sparrow of different hatching times and eggsizes, were of eggs.Lines indicate +2 SE. Sample sizes are males = 147, females = 147. equal size on Day 2 of the nestling period. Six days later all 17 males were larger than their sisters and their mean weight was significantly egg volume and sex ratio which might serve to greater (matched t = 5.40, P < 0.001; Table 2). bias the between-clutch data. Sexual differencesin growth rates would thus be In terms of the Trivers-Willard (1973) hy- expectedto enhance rather than reduce any size pothesis,differences in eggsize have significance differencesbetween male and female hatchlings. only to the extent that they reflect differencesin Several factors could potentially bias our re- offspring quality and ultimate reproductive suc- sults. In White-crowned Sparrows, as in many cess.Unfortunately such parameters are exceed- birds, average egg size tends to increase with or- ingly difficult to test in the field. Instead we must der of laying (Mead and Morton 1985). A ten- make use of the indirect argument that greater dency for later-laid eggsto be male could sec- egg size for males cannot be related to ultimate ondarily result in a larger average size for male reproductive successif eggsize doesnot correlate eggs. When we compared egg sex with laying with hatchling size, or if female nestlings grow order for all eggs in which both were known, faster than their male siblings thereby countering however, there was no tendency for eggslaid later the initial advantages of larger egg size. in the clutch to be male (x2 = 2.64, P > 0.05;

TABLE 1. Mean egg volume (cc) for male, female, and all White-crowned Sparrow eggsmeasured. P values refer to differencesbetween mean volumes of male and female eggs.

Egg volume, R k SD (n) YetI1 All eggs Males Females P

1981 2.990 f 0.220 (118) 2.978 + 0.190 (27) 2.896 k 0.269 (20) >0.05 1982 2.990 + 0.240 (151) 3.084 k 0.213 (29) 3.030 k 0.220 (43) >0.05 1983 2.935 + 0.236 (176) 3.011 k 0.237 (29) 2.965 + 0.232 (29) >0.05 1984 2.985 k 0.270 (112) 3.124 + 0.256 (41) 3.000 + 0.299 (41) >0.05 1985 3.040 -t 0.250 (67) 3.059 f 0.221 (21) 3.019 + 0.304 (14) >0.05 All years 3.060 f 0.232 (147) 2.990 -+ 0.262 (147)

Table 3). Indeed, there were more males than TABLE 3. Number of male and female eggsby laying females among the first two eggslaid. order in four-eggclutches of Mountain White-crowned In some nests it was not possible to sex every Sparrows. chick. This too could bias our results if there was Laying order a tendency not to sex either females from large Eggs 1 and 2 Eggs 3 and 4 eggs or males from small eggs. Several factors argue against such bias. First, mean volume Males 50 52 Females 32 54 was nearly identical for sexed and unsexed eggs, 3.02 & 0.20 cc and 3.01 + 0.22 cc, respectively. Second,when considered as a group, the reasons for failing to sexeggs are unlikely to have selected in the production of unisex clutches (Williams for eggsthat were at once both a particular size 1979, Fiala 198 la). Clearly field data for birds and sex. There were 58 unsexedeggs from clutch- have failed to confirm this prediction (Harmsen es in which other chicks were sexed. The num- and Cooke 1983). It may be, however, that the bers and reasons for not sexing are as follows: assumption underlying this prediction is in error. failed to hatch (2 l), chicks disappearedfrom nest Unisex clutchescan be expectedif offspringqual- before age of possible fledging (1 l), nest subject ity within a clutch will be consistently better or to partial depredation (7), chick could not be worse than the mean for the population. In fact, associatedwith a specific egg (7) chicks fledged as already noted, offspring quality varies widely before laparotomy (5) laparotomy was incon- between siblings from the same clutch. clusive because of bleeding (5) egg was broken Our data indicate that in White-crowned Spar- during handling (2). rows male eggsare larger than female eggs.To Previous reports in the avian literature have our knowledge, this is the first demonstration of varied widely in their support of the Trivers- sexual dimorphism in avian egg size. We also Willard hypothesis. Field studies have demon- report that larger eggsproduce larger hatchlings strated seasonalvariations in primary sex ratio and that male nestlings grow faster than females. of both Common Grackles, Quiscalus quiscula These latter findings have been documented in (Howe 1977), and Yellow-headed Blackbirds, a number of other species(Parsons 1970, 1975; Xanthocephalusxanthocephalus (Patterson and Nisbett 1973; Schifferli 1973; Howe 1976; Nolan Emlen 1980). In each case the observed trends and Thompson 1978; Fiala 1981b; Bancroft were postulatedto coincide with seasonalchanges 1984) and together they support the suggestion in food supply. Ryder (1983) has reported non- that larger egg size may be of some significance random distribution of the sexes according to in determining adult quality. Our findings are laying order in clutchesof Ring-billed Gulls (Lar- not without contradiction. Weatherhead (1985) us delawarensis). Ankney (1982) has published has similarly examined egg size and sex in Red- similar findings for Lesser Snow Geese (Chen winged Blackbirds (Agelaiusphoeniceus). Inter- caerulescens),but these could not be confirmed estingly, he too found that male eggswere larger by a larger study (Cooke and Harmsen 1983). than female eggsin four-eggclutches in both years On more theoretical grounds, Myers (1978) has of his study. As in our study, the degree of dif- criticized the Trivers-Willard hypothesisfor fail- ferencewas not statistically significant in any one ing to consider the costs of facultative manipu- year. Our analysis differs in that we combined lation. Although adjustment of postconception data from several years. sex ratios through sex-specificmortality may in- While our results can be predicted on the basis deed be costly (Burley 1982), adjustment of the of the Trivers-Willard hypothesis, they should primary sexratio need not be. In birds the female not necessarily be taken as evidence for facul- is the heterogamete (Sturkie 1986), and sex is tative manipulation of sex at this time. First, it determined when the follicle undergoesmeiosis. is essentialto measure the effectin nature, if any, Becauseone-half of the ovum’s genome is nor- that small differences in egg size have on adult mally discarded in the polar body, nonrandom quality. The task of relating parental investment segregationof sex chromosomes during meiosis to ultimate reproductive successof offspring re- could allow for manipulation of offspring sex mains a major challenge for all tests of this hy- without significant cost. Finally, it has been ar- pothesis. Second, there is much to be learned gued that facultative manipulation should result about the mechanisms of sex determination and 802 P. S. MEAD, M. L. MORTON AND B. E. FISH egg provisioning. Specifically, it is necessaryto of this manuscript. Funding was provided by a Na- determine whether the observed size difference tional Science Foundation Graduate Fellowship and Occidental College. reflectsmanipulation of eggsex according to provisioning or simply greater provisioning of male LITERATURE CITED eggsin a species,such as White-crowned Spar- ANKNEY, C. D. 1982. Sex ratio varies with egg se- rows, where adult males are larger. Data cur- quence in Lesser Snow Geese. Auk 99:662-666. rently available indicate that in birds sex deter- AR,A.. AND H. RAHN. 1980. Water in the avian eaa: mination occurs when the follicle undergoes overall budget of incubation. Am. Zool. 20:37‘jl meiosis about 3 to 4 hr before ovulation (Olsen 384. and Fraps 1950, Sturkie 1986). At this time the BANCROFT,G. T. 1984. Patterns of variation in size of Boat-tailed Grackle Quiscalusmajor eggs.Ibis yolk of the egg has been deposited (Lehrman 126496-509. 196 1; Gilbert 1970, 197 1). In at least one altricial BAPTISTA,L. F., AND M. L. MORTON. 1982. Song and several precocial species,yolk size is pro- dialects and mate selection in Montane White- portional to final egg size (Romanoff and Ro- crowned Sparrows.Auk 99537-547. BURLEY,N. 1981. Sex ratio manipulation and selec- manoff 1949, Parsons 1970, Howe 1978, Rick- tion for attractiveness.Science 211:721-722. lefs et al. 1978) suggestingthat final egg size is BURLEY,N. 1982. Facultative sex-ratio manipula- in effect determined prior to egg sex. If this is tion. Am. Nat. 120:81-107. true in White-crowned Sparrows, our results CAREY,C. 1986. Tolerance of variation in eggshell would suggest manipulation of the sex-deter- conductance,water loss,and water content by red- winged blackbird embryos. Physiol. Zool. 59: 109- mining meiotic division (see Howe 1977 and 122. Ankney 1982 for discussionsof nonrandom sex CHARNOV,E. L., R. L. LOS-DENHARTOGH, W. T. JONES, determination). Alternately, there could be dif- ANDJ. VAN DEN ASSEM. 1981. Sex ratio evolution ferential deposition of albumin in male eggsafter in a variable environment. Nature 289:27-33. CLUTTON-BROCK,T. H. 1982. Sons and daughters. ovulation. This deceptively simple explanation Nature 298: 11-12. would require transcription and translation of a COOKE,F., AND R. HARMSEN. 1983. Does sex ratio sex-specific gene, along with a differential re- vary with eggsequence in LesserSnow Geese.Auk sponseby the oviduct, all before the first cleavage 100:215-217. of the zygote (Olsen 1942). If it occurs, such an DARWIN,C. 1871. The descentof man, and selection in relation to sex. John Murray, London. early gene expression might prove of interest to DEWOLFE,B. B. 1968. Zonotrichia leucophrysorian- those studying gene expression during develop- tha: Mountain White-crowned Sparrow, p. 1338- ment (Mtiller et al. 1984, Rubin et al. 1986). 1343. In 0. L. Austin [ed.], Life historiesof North Finally, we suggestthat discrepancies within American cardinals,grosbeaks, buntings, towhees, finches,sparrows, and allies. U.S. Natl. Mus. Bull. and between studies of the Trivers-Willard hy- 237 pothesis may be due in part to excessive em- FIALA, K. L. 1981a. Sex ratio constancyin the red- phasis on sex ratios and to the neglect of factors winged blackbird. Evolution 35:898-910. which operate within each brood to modify the FIALA. K. L. 198lb. Renroductive cost and the sex ratio in red-winged blackbirds, p. 198-2 14. In R. reproductive potential of siblings. Emphasizing D. Alexander and D. W. Tinkle [eds.], Natural the latter, we have obtained results that are con- selectionand social behavior: recent researchand sistent with the hypothesis. Many factors, op- new theory. Chiron Press, New York. erating simultaneously and in complex ways, may GIBB,J. 1950. The breeding biology of the Great and influence the reproductive successof offspring Blue titmice. Ibis 92:507-539. GILBERT,A. B. 1970. Yolk deposition in the chicken (Burley 1982). It may be essential, therefore, to oocyte and its relationship with ovulation. J. Re- consider simultaneously such factors as eggsize, prod. Fertil. 23:539-540. hatching order, time of season,and parental at- GILBERT,A. B. 1971. The ovary, p. 1163-1708. In tractiveness (Burley 198 1, 1982; Immelmann et D. J. Bell and B. M. Freeman [eds.], Physiology al. 1982, Thissen and Martin 1982) when testing and biochemistry of the domestic fowl. Vol. 3. Academic Press,New York. for facultative manipulation. HAMILTON,W. D. 1967. Extraordinary sex ratios. Science 156:477-488. ACKNOWLEDGMENTS HARMSEN,R., AND F. COOKE. 1983. Binomial sexratio distribution in the LesserSnow Goose: a the- For assistancein the field and laboratory we thank M. oretical enigma. Am. Nat. 121: l-8. Alego Gilsdorf, A. Lee, M. Pereyra, and S. Warschaw. HERRE,E. A. 1985. Sex ratio adjustment in fig wasps. We thank T. Clutton-Brock, R. Mead, K. Rassbach, Science 228:896-898. and P. Sherman for their comments on an earlier draft HOWE, H. F. 1976. Egg size, hatching asynchrony, SEXUAL DIMORPHISM IN EGG SIZE 803

sex, and brood reduction in the Common Grackle. OLSEN, M. W., AND R. M. FRAPS. 1950. Maturation Ecology 57:1195-1207. changesin the hen’s ovum. J. Exp. Zool. 114:475- HOWE,H. F. 1977. Sex-ratio adjustment in the Com- 489. mon Grackle. Science 198:744-746. PARSONS,J. 1970. Relationship between egg size and HOWE, H. F. 1978. Initial investment, clutch size, post-hatchingchick mortality in the Herring Gull and brood reduction in the Common Grackle (Laws urgent&us). Nature 228: 1221-1222. (Quiscalusquiscula L.). Ecology 59: 1109-l 122. PARSONS,J. 1975. Asynchronoushatching and chick HOYT, D. F. 1979. Practical methods of estimating mortality in the Herring Gull Larus argentatus. volume and fresh weight of bird eggs.Auk 96:73- Ibis 117:517-520. 77. PATTERSON,C. B., ANDJ. M. EMLEN. 1980. Variation IMMELMANN,K., J. P. HAILMAN, AND J. R. BAYLIS. in nestling sex ratios in the vellow-headed black- 1982. Reputed band attractivenessand sex ma- bird. Am-Nat. 1153743-747. nivulation in Zebra Finches. Science2 15~422. PINKOWSKI.B. C. 1975. Growth and develooment of KEND&, S. C. 1941. Length of day and energy Eastern Bluebirds. Bird-Banding 46:272:289. requirementsfor gonad development and egg-lay- PINKOWSKI,B. C. 1979. Effect of nesting history on ing in birds. Ecology 22:237-248. egg size in Eastern Bluebirds. Condor 8 1:210. KENDEIGH,S. C., T. C. KRAMER,AND F. HAMERSTROM. RICKLEFS,R. E. 1965. Brood reduction in the Curve- 1956. Variationsin eggcharacteristics ofthe House billed Thrasher. Condor 67:505-5 10. Wren. Auk 73142-65. RICKLEFS,R. E., D. C. HAN, AND W. A. MONTEVECCHI. KLOMP,H. 1970. The determination of clutch size 1978. The relationshipbetween eggsize and chick in birds. A review. Ardea 58:1-124. size in the LaughingGull and JapaneseQuail. Auk LACK, D. 1954. The natural regulation of animal 95:135-144. numbers. Oxford Univ., London. ROMANOFF,A. L., AND A. J. ROMANOFF. 1949. The LEHRMAN,D. S. 1961. Hormonal regulation of pa- avian egg. John Wiley and Sons, New York. rental behavior in birds and infrahuman mam- RUBIN, M. R., L. E. TOTH, M. D. PATEL,P. D’EUSTA- mals, p. 1268-1382. In W. C. Young [ed.], Sex CHIO,AND M. C. NGUYEN-HUU. 1986. A mouse and internal secretions. Williams and Wilkins, homeo box geneis expressedin spermatocytesand Baltimore. embryos. Science 233~663-667. MAYOH, K. R., AND R. ZACH. 1985. A new method RYDEN, 0. 1978. Egg weight in relation to laying for matching hatchlings with their eggs. Condor sequencein a south Swedish urban population of 87:300-301. the Blackbird Turdusmerula. Omis Stand. 9: 172- MEAD, P. S., AND M. L. MORTON. 1985. Hatching 177. asynchronyin the Mountain White-crowned Spar- RYDER,J. P. 1983. Sex ratio and egg sequence in row (Zonotrichia leucophrysoriantha): a selected Ring-billed Gulls. Auk 100:726-730. or incidental trait? Auk 102:781-792. SCHIFFERLI,L. 1973. The effect of egg weight on the MOLLER,M. M., A. E. CARRASCO, AND E. M. DE- subsequentgrowth of nestling Great Tits Parus ROBERTIS.1984. A homeo-box-containing gene major. Ibis 115:549-558. expressedduring oogenesisin Xenopus. Cell 39: STURKIE,P. D. 1986. Avian physiology. Springer- 157-162. Verlag, New York. MYERS,J. H. 1978. Sex ratio adjustment under food THISSEN,D., AND E. MARTIN. 1982. Reputed band stress:maximization of quality or numbers of off- attractiveness and sex manipulation in Zebra spring?Am. Nat. 112:381-388. Finches. Science2 15:423. _ NISBET~,I.C.T. 1973. Courtship-feeding,egg-size and TRIVERS,R. L. 1978. The evolution of reciprocal al- breeding successin common terns. Nature 241: truism, p. 189-226. In T. H. Clutton-Brock and 141-142. P. H. Harvey [eds.], Readingsin sociobiology.W. NOLAN, V., JR., AND C. F. THOMPSON. 1978. Egg H. Freeman and Co., San Francisco. volume as a predictor of hatchling weight in the TRIVERS,R. L., AND D. E. WILLARD. 1973. Natural Brown-headedCowbird. Wilson Bull. 90:353-358. selection of parental ability to vary the sex ratio O’CONNOR,R. J. 1975. Initial size and subseouent of offsvrina. Science 179190-92. growth in passerine nestlings. Bird-Banding 46: WEATHERH~AD~P.J. 1985. Sex ratios of Red-winged 329-340. Blackbirds by egg size and laying sequence.Auk OJANEN,M., M. ORELL,AND R. A. VAISANEN. 1979. 102:298-304. Role of heredity in egg size variation in the Great WERREN,J. H. 1980. Sex ratio adaptations to local Tit Parus major and the Pied Flycatcher Ficedula mate competition in a parasiticwasp. Science209: hypoleuca.Omis Stand. 10:22-28. 1157-l 159. OJANEN,M., M. ORELL,AND R. A. VAISANEN. 1981. WILLIAMS,G. C. 1979. The question of adaptive sex Eggsize variation within passerineclutches: effects ratio in outcrossedvertebrates. Proc. R. Sot. Lon- of ambient temperature and laying.-. sequence.Or- don B Biol. Sci. 205:567-580. nis Fenn. 58:93-108. ZACH,R. 1982. Hatchingasynchrony, egg size, growth, OLSEN,M. W. 1942. Maturation, fertilization and and fledging in Tree Swallows. Auk 99:695-700. early cleavage in the hen’s egg. J. Morphol. 70: 513-528.