Some Problems and Approaches in Avian Mate Choice

SOME PROBLEMS AND APPROACHES IN AVIAN MATE CHOICE

KRISTINEJOHNSON •'3 AND JOHN M. MARZLUFF2'4 •Departmentof Biology,University of New Mexico,Albuquerque, New Mexico87131 USA, and 2Departmentof BiologicalSciences, Northern Arizona University, Flagstaff,Arizona 86011 USA

ABSTP,•CT.--Moststudies of mate choice in birds consider questionssuch as the existence of mate choice, which traits are preferred, and how the preferencesevolved. In order to answer these questions,it is necessaryto distinguishbetween pairs of key processessuch as dominanceand choice,assortative mating and type preference,or male choice and female choice. We review these and other difficulties in the study of avian mate choice. As an illustration of methodologicalissues, we discussour work on Pinyon Jays (Gymnorhinus cyanocephalus).Males that were successfulin mate-choiceexperiments were more brightly coloredand had large testes,but were not necessarilylarger or dominant.Preferred females were large, dominant,and had thicker bills. In flee-living populations,smaller than average malesand larger than averagefemales lived longer. Pairscomposed of small malesand large femaleshad sonswith higher fecunditiesand greater survivorship.We suggestthat many ornithologistscould combinetheir long-term field observationswith controlledexperiments to profitably study mate choice.Received 27 January1989, accepted 6 November1989.

THE AREAof sexual selection is currently one evolved. The considerabletheory in this area of the most controversial and rapidly devel- offersnumerous questions for empiriciststo ad- oping in biology (Andersson and Bradbury dress(Heisler et al. 1987). Empirical studiesof 1987).There is a large body of theory on sexual female choiceusually begin with the question selection;and an increasingnumber of empir- of whether female mating preferencesfor par- ical studies, particularly of mate choice, focus ticular male traits exist. on birds (e.g. Komersand Dhindsa 1989, Zuk Identifyingtraits.--The first difficulty in in- et al. in pressa, b). Empirical studiesoften fail vestigating mate choiceis to decide which traits becausethey do not addressimportant theo- might be important. If there are field data for retical questions,their methodology does not the speciesof interest, one can identify traits allow discrimination of key processes,or both. used in courtship displays,search for correla- Our discussionof the first problem is brief, as tions between specifictraits and mating or re- this topic is reviewed in detail elsewhere (Ar- productive success,or look for assortative mat- nold 1985, Bradbury and Andersson 1987). We ing with respectto specific traits. These traits focus here on commonly encountered meth- suggesta starting point for experimentalstudy. odologicaldifficulties in the empiricalstudy of If there are no relevant field data, theory and avian mate choice. We suggestapproaches to common sense can suggest traits for experi- these problems and provide an example from mentation. Ideally, one should then go to the work with captive and free-living Pinyon Jays field to determine the fitness consequencesfor (Gymnorhinuscyanocephalus) that illustratessome individuals with the preferred traits. of these methodologicalissues. Is matingnonrandom?--Once appropriate traits have been identified, it is necessaryto docu- DIFFICULTIES IN THE STUDY OF MATE CHOICE ment nonrandom mating for the traits of interest. Standard statisticalprocedures can be ap- A central theoretical question is how female plied to the results of laboratory experiments. choicecan affect the evolution of secondarysex In the field, however, it can be unclear whether characteristics.Closely associatedis the ques- an observedpattern is the result of preferences tion of how the mating preferencesthemselves for a particular trait (type preference;Burley 1983) or prevalence of that trait in the pool of 3 Current address:Department of Ecology,Etholo- prospective mates at the time mating occurs gy, and Evolution, University of Illinois, 606 East (Cooke and Davies 1983). For example, in sev- Healey, Champaign, Illinois 61820 USA. eral bird species,the ages of partners are cor- 4 Current address:Star Route Box 2905, Dryden, related (Reid 1988). Reid (1988) has shown that, Maine 04225 USA. with stable pair bonds, such correlations can

296 The Auk 107: 296-304. April 1990 April 1990] AvianMate Choice 297 occur in the absenceof mate choice, through 1986). Males should be isolated visually and random mating alone. physicallyto prevent dominantsfrom inhibit- To investigate apparent nonrandom mating ing subordinatedisplay behavior (Komersand patterns, it is not appropriate to apply standard Dhindsa 1989). statistical procedures (such as Chi-square ap- Alternatively, it may be necessaryto choose proximationsor correlationanalyses) to the traits experimental design and analysis that allow of a free-living population of existingpairs, be- separationof the effectsof choice and compe- causethese tests require that different pair bonds tition, without physically separatingcompeti- form independently. Mate pools are finite, and tors. Pinyon Jaysare highly social and do not once two individuals in a finite mate pool pair, behave normally when isolated in captivity. the remaining individuals have reducedchoices Thus, mate-choice trials must be run without that depend on previous choices.In monoga- isolatingmales. Johnson (1988a) determined the mous species,this continuesuntil the last two males (and their traits) that were successful in individuals have no choice but to pair with one male-male competition (i.e. male dominance) in another. Such clearly dependent eventscannot the absence of females, and then females were be analyzed with parametric or nonparametric allowed to chooseamong several males that were tests of association. not separatedphysically. In thesefemale choice Randomization procedures can avoid this experiments,female choiceand male-malecom- problem by comparing all possible (random) petition operated simultaneously. There are pairings at a given time with the pairings ac- severalpossible outcomes with this type of de- tually observed (Marzluff and Balda 1988b, sign. First, the same males may be successful Johnstonand Johnson1989). For this approach, when male-male competitionacts alone aswhen it is necessaryto know which individuals were male competition and female choice occur si- available in the mate pool at the beginning of multaneously.This outcomeindicates that male- the pairing period and calculatethe N! possible male competition is the primary factor that de- patterns that can be formed between N males termines male mating success.Second, when and N females. Nonrandomness of the observed female choice is introduced, additional males pairing pattern is calculatedby determining how or traits may be favored.This indicatesthat both rare that pattern is relative to all possible pat- competition and choice affect male mating suc- terns. cess.Third, entirely different malesor traitsmay Factorsconfounding choice.--To decide wheth- be favored in the male-male competition and er nonrandom mating patternsare the result of male competition-female choice trials. This re- mate choice,it is necessaryto rule out the pro- suit implies that female choice operatesin the cessof intrasexualcompetition as a complicat- presence of male-male competition and that ing factor. Consider female choice of males in male-male competition does not override the a typical nonterritorial speciesin which males operation of female choice. In Johnson'sexper- usually show behavioral dominanceto females. iment, male competition alone appeared to fa- If nonrandom mating occurs,it can be unclear vor different birds and male traits from male whether the mating pattern is a result of female competition and female choice acting simulta- preference for certain male types or whether neously.This suggestedthat female Pinyon Jays intra-male competition allows dominant males exercisetheir preferences,even in the presence to monopolize accessto females. Even when of males,who are usually dominant to females. femalesappear to choosemales, male-male com- Similar logic was used by Komersand Dhindsa petition can mediate female choice. For exam- (1989) for Black-billed Magpies (Pica pica) in ple, female American Wigeons(Anas americana) captive flocks.When either of the first two con- matemore often with larger,heavier adult males ditions occurs, however, the effects of choice in full alternate plumage, but these males also and competition are indistinguishable. When- tend to be dominant (Wishart 1983; see also ever possible, it is simpler to separatecompet- West et al. 1981, for Brown-headed Cowbirds, itors at the outset of the experiment. Molothrus ater). We have suggestedways in which intrasexual The easiestway to eliminate the effectsof competition can be distinguished from female male-male competition is to experimentally re- choice;however, nonrandom patterns of mat- strict malesfrom competing(e.g. Burley 1981a, ing may alsoresult from female and male choice 298 JOHNSONAND MARZLUFF [Auk, Vol. 107

operating simultaneously.In speciesin which or functional, choices on the basis of resources, both malesand femalesinvest in offspring,both parental investment, or genes. By definition, sexesshould be selective (Trivets 1972). High- functional mate choiceprovides fitness benefits quality individualsshould be morechoosy than to the chooser. An alternative is that birds choose low-quality individuals (Burley 1977). High- mates on the basis of aesthetic traits that confer quality birds should pair assortatively,which no advantage on the chooser (Burley 1986, leaveslow-quality birds to pair with eachother. Brodsky1988). Genetic modelsof runaway sex- This can give the appearanceof assortativemat- ual selection have shown that nonfunctional ing with respect to the traits of interest, when preferencesmay evolve becauseof correlations in fact the pattern resultsfrom both sexeshav- that developbetween the genesfor the female's ing type preferences for high-quality mates preferenceand the genesfor the preferred male (Burley 1983).The bestway to avoid this fallacy trait (Lande 1981, Kirkpatrick 1982). is with controlled experimentsin which only It is reasonable to assume that females that one sex is allowed to choose at a time, to de- pair with territorial malesare free to choose.It termine preferred traits and the strengths of can be difficult to determine what benefits fe- preferencesfor both sexes(Burley 1981a,1986; malesderive from being selective.In the many Johnson 1988a, b). speciesthat defend type A territories, females Whether examining naturally varying or ar- may simultaneouslyreceive resources,parental tificial traits, there are two basicapproaches to care, and genes from males. It can be difficult mate-choice experiments. Numerous studies to determine which, if any, is most important. have taken a univariate or bivariate approach, In addition, features of the male and the ter- and examined only one (Yosef and Pinshow ritory are often correlated (e.g. Searcyand Ya- 1989) or two (Duncan and Bird 1989, Komers sukawa 1983, Alatalo et al. 1984, Price 1984). and Dhindsa 1989) traits. With this approach, Red-winged Blackbirds (Agelaiusphoeniceus) it is bestto match choicebirds for all exceptthe represent a case in point. After several years trait of interest (Burley 1981a, 1986). A poten- and many careful studies(a partial list includes tially more informative approach is to select Searcy 1979; Lenington 1980; Yasukawa et al. ct•oicebirds randomly, measureall traits that 1980, 1987; Searcy and Yasukawa 1981, 1983; might be relevant, and analyze several mea- Yasukawa 1981), most workers agree that ter- sured traits simultaneously with multivariate ritory quality is an important criterion for fe- procedures (Johnson 1988a, b; Johnston and male choice, but the influence of male attri- Johnson1989; Zuk et al. in pressa). butes, especially parental care and genetic Use of nonindependent observations is a contribution, is still open to question (Weath- commonproblem with experimentalstudies. If erhead and Robertson 1979; Searcy and Yasu- a subject(e.g. a choosingfemale) is usedin more kawa 1981, 1983; Searcy 1982; Eckert and than one trial in the sameexperiment, her two Weatherhead 1987; Yasukawa et al. 1987). When choicesshould not be consideredindependent male and territory qualities are not correlated, data points. Similarly, caution must be used in the two can be examined independently. For re-using stimulus birds within the same exper- example,in Pied Flycatchers(Ficedula hypoleu- iment. The details of experimental design in ca),nest boxes were manipulatedto controlmale mate-choiceexperiments are beyond the scope settling pattern. This disrupted the male-terri- of this paper, but workers should avoid faulty tory correlation that developswhen the first- designsthat could invalidate results (Hurlbert arriving, older males have accessto the pre- 1984, Kroodsma 1989). ferred boxes (Alatalo et al. 1986). In territorial or lekking species,female choice Another approach to the confounding prob- may operateindependently, because females are lem of territory quality is to use each male, be- free to move from one more or less stationary fore his traits are altered, as his own control male to another. In territorial specieschoice for (Andersson 1982). An advantage of this ap- a male can be confused with choice for his ter- proach is that an individual trait can be manip- ritory. ulated, which controls for correlated traits. With Why choosemates?--Once it is clear that mate adequatesample sizes,territorial males can be choice,and not simply intrasexualinteraction, manipulatedrandomly, which randomizesthe results in nonrandom mating, it is important to effects of territory quality on female choice. know how the preferencesevolved. The nature Changesin mating successof manipulatedmales of the preferred trait indicateswhether or not are then assumedto be due to the manipulation choice is functional. Birds can make adaptive, rather than territory quality. Where mate choice April 1990] AvianMate Choice 299 is resource-based,quality of resourceson the ural populations(Van Noordwijk 1984, Hail- territory can be manipulated (Yosef and Pin- man 1986). For breeding studies,samples usu- show 1989). ally must be sizable and relatednessbetween In specieswhere malesprovide parentalcare individuals known. For these reasons,genetic but do not defend resources on which females studiesshould be undertaken only after careful can basea choice, choice is based on male qual- planning (Heisler et al. 1987). ities.The problemis to distinguishamong choice Burley (1981b, 1986)has pointed out the po- for parentalqualities, good genes, and arbitrary tential for birds to choose mates and allocate attractiveness (Johnson 1988a). Several studies reproductive effort based on aesthetic traits. have shown that male parental investment in- With few exceptions(Watt 1982,Brodsky 1988, creasesfemale reproductive success(Patterson Hagan and Reed 1988), field-workers have not et al. 1980, Alatalo et al. 1981, Catchpole et al. testedthe effectsof color bandson reproductive 1985, Leonard and Picman 1988). To show func- success.If band colorsare applied randomly in tional female choice for male parental qualities the field, differential mating successor nonran- requiresalso finding male traits that indicate in dom mating by band color may indicate that advanceparental investment and showing that the birds respondto artificial aestheticmarkers. females prefer those traits (e.g. Eckert and Laboratory experiments can be used to inves- Weatherhead 1987, Yasukawa et al. 1987). tigate this possibility (Burley 1986). Workers In lekking species,the investigatormust dis- who experiment on mate choice for naturally tinguish between mate choicefor good genes varying traits should avoid the potential com- and arbitrary (aesthetic) choice. To test good plicationscaused by color-marking experimen- geneshypotheses, it is necessaryto show that tal birds. Likewise, field-workers should either male attractivenessis correlatedwith viability control for this confounding effect or use large of malesor their offspring.For birds,this means samplesizes and take care to apply color bands that both mate-choice experiments and field randomly. studiesmay be required. If no relationship exists between male traits One criticismof the good-geneshypothesis and male mating success,it is reasonableto re- is that sexualselection for goodgenes will even- ject the existence of female choice of males tually reduce heritable variation in the pre- (Lightbodyand Weatherhead1987, Leonard and ferred traits until it becomes so low that no Picman 1988).There are severalpotential prob- benefitresults from choicefor genes(Maynard lems with the conclusion that mate choice does Smith 1978, Searcy 1982). Showing heritable not occur. First, it is difficult to be certain that variation for the preferred traits would counter all relevant traits were measured. Second, fe- this criticism.Alternatively, it is possiblethat males may have preferencesbut may exercise indicator traits such as secondarysex charac- them only when appropriatechoices are offered teristicsare facultatively influenced by envi- (Zuk et al. in pressb), or when male competition ronmental factors like disease (Hamilton and does not constrain female choice. Zuk 1982).In this case,heritability of indicator We believe that measuringmale traitsvs. mat- traits is expectedto be low, while phenotypes ing successin a free-living population of a typ- reflect physiologicalcondition, and overall fit- ical territorial, monogamousspecies is unlikely ness remains heritable. to producenew insightsinto avian mate choice. Somemodels of runawaysexual selection (ar- A combinationof laboratoryexperiments to dis- bitrary choice) require the development of a tinguish among confounding influences and genetic correlation between females' prefer- field measurementsto allow meaningful inter- encesand males'traits in order for femalepref- pretationof experimentaldata will usuallyprove erenceto evolve(Lande 1981, Kirkpatrick 1982). productive. To test hypothesesof the evolution of female mating preference,it is necessaryto know if A CASE STUDY femalepreferences are heritable.Investigation of heritabilities and genetic correlationsre- Mate choicein PinyonJays.--Pinyon Jaysmain- quires the techniquesof quantitativegenetics, tain largeflocks and nestin loosecolonies. There which were not developed for use in natural is ample potential for individuals to compare populations.Environmental heterogeneity, ge- prospective mates (Balda and Bateman 1971, notype-environment interactions, positive as- 1972).Pinyon Jaysform monogamous,lifelong sortativemating, and other factorscan strongly pair bondsand separationis almostnonexistent affectthe estimationof thesequantities in nat- (Marzluff and Balda 1988a). Becauseboth males 300 JOHNSONAND M.•oamul•l• [Auk,Vol. 107 and females make large parental investments, feedingstations. Reproductive success of pairsand both sexes should be selective about their mates. their offspringwas determined each breeding season Mate choice is not confoundedby territory (details in Marzluff and Balda 1988b). We used these quality becausePinyon Jaysdo not defend a data to investigatereproductive success of pairswith breeding territory (Balda and Bateman 1971, traits shown to be preferred in the lab. Pairs were Bateman and Balda 1973). Males are ca. 13% classifiedaccording to whether partnerswere heavy, meaning heavier than the mean for individuals of heavier than femalesand have larger bills (Li- that sexin the Flagstaffpopulation, or light,meaning gon and White 1974). Male plumage is gener- equal to or lighter than the mean. ally brighter than female plumage, although there is considerableoverlap. The sexual di- morphism, male-biased sex ratio (60:40, Mar- RESULTS zluff and Balda 1988c) and some results of mate-choice experiments suggest that sexual Femalechoice of males.--Male desirability selectionmay operatemore strongly on males scoresfell into three clear groups: males that than on females (Johnson 1988b). were never successful with females, males that We discussresults of two separatestudies of were sometimes successful, and those that were Pinyon Jays.One was a long-term field study highly successful.Univariate and multivariate performed by R. Baldaand his colleagues,the analysesof variance were used to determine othera laboratorymate-choice study conducted which traits were preferred by females.Malar by K. Johnson.Most of the data discussedare feather brightnessand testis length differed presentedin detail elsewhere.We presentsum- among the three groupsof males by the uni- maries of thoseanalyses, along with somenew variate tests, and the MANOVA for all mea- data. We discussgeneral conclusionsfrom both sured traits indicated that the three groupsdif- studiesto illustrate methodologicalissues. fered in a linear combination of all variables. All possiblecontrasts were significant at the P METHODS < 0.05 level. Females preferred males with brighterplumage and larger testes,but they did Mate-choiceexperiments.--Wild-caught Pinyon Jays not prefer larger males nor males having the were housed in large aviaries on the roof of the Uni- traits important in male-male competition versityof New Mexicobiology building. Johnson cap- (Johnson 1988a). Testis size was not correlated tured males and females at different localities, to en- with overall body size. sure that males and females would be unfamiliar with Male choiceof females.--A stepwisemultiple one another, and housed them in separateaviaries. Forty-one female choice trials were conducted, in regressionof the female traits on female desir- which eachfemale was allowed to chooseamong three ability gave five significantregression models. (1986) or two (1985) malesand to perform courtship. The bestone-variable model was body weight, A similar male choiceexperiment (n = 26) in which the best two-variable model included weight males chose among three (1986) females was per- plus dominance rank, and the best three-vari- formed. Choiceexperiments were done in a smaller able model was weight plus rank plus bill thick- experimental aviary, and dominance rankings of ness. All three partial regression coefficients choicebirds were determinedbefore the trials began. were significant for the three-variable model Theserankings agreed with dominancerankings of and step 3 contributed a significant increment birds when they were in the large aviaries. Choice birds all wore two yellow bands (two on the right to the total R2. Significancedecreased beyond leg, two on the left, or one on eachleg), and choosers the three-variablemodel to becomenonsignifi- were unbanded.Desirability scoreswere computed cant for steps 6-9. Thus, body weight, domi- for each individual, based on the number of times nance rank, and bill thickness were related to eachbird performedcourtship and was chosenin the the likelihoodof femalesbeing chosenby males experiments.Each bird wasmeasured for weight, tar- (Johnson 1988b). sus,wing length, bill length, and bill thicknessand Reproductivesuccess of free-livingpairs.--The compared with museum specimensto score it for data of Marzluff and Balda(1988b) suggest that brightnessof head and malar feathersand size of the the pairs that remained together longest were white throat patch.Laparotomies were performedto light (male)-heavy(female) pairs (Table 1; trends confirm sex and allow measurement of testes (see Johnson[1988a, b] for details of methods and statis- are evident, but samplesizes did not allow hy- tics). pothesis testing). Becauseof slight sexual di- Observationsof free-livingbirds.--A flock of color- morphism,a male that is much lighter than av- banded, known-aged Pinyon Jaysnear Flagstaff,Ar- erageand a female that is heavier than average izona, was monitored from 1972 to 1986 as it visited will be closeto the sameweight. In contrast,a April1990] Avian Mate Choice 301

T^nI•l•1. Fitnessmeasures (• _+SE) of four typesof PinyonJay pairs, classified according to mass.H = heavier than the meanfor that sex;L = lighter than the meanfor that sex.Sample sizes are in parentheses.a Bodymass Lifespan Fitnessof sons Male Female Male Female Fecundity Longevity H H 5.75 + 0.48(4) 6.44 + 1.24(9) 0.00 (I) 4.00 _+0.00 (I) H L 3.50 + 1.50(2) 5.33+ 1.76(3) 0.67 ñ 0.33(3) 5.00 + 1.41(4) L H 8.44 + 1.30(9) 7.75 + 0.65(8) 2.00 4- 0.63(5) 5.33 + 1.05(9) L L 6.44 + 0.50(9) 6.50 + 0.48(6) 0.88 + 0.30(8) 4.07 + 0.55(14) ' Descriptivestatistics aregiven without hypothesis testing because ofsmall and unequal sample sizes (excerpt from Marzluff and Balda 1988a); birdswith incomplete life historiesaccount for discrepancies in number of birdsin differentweight classes. heavy(male)-light (female) pair will havea large ences for the above traits, see Johnson 1988a, weight difference.Over all pair types,male life- b). span was significantly negatively correlated Light males and males mated to heavy fe- with weight differences(male-female) between males lived longer. This may mean that there partners(r = -0.28, P = 0.043, n = 24). Light is a survival advantagefor a male that is mated malesappeared to live longer than heavy males, to a heavy female. For example,a male with a and regardlessof weight, malesmated to heavy relatively large, aggressivemate might have to femalesappeared to live longer (Table 1). expend less energy assistingthe smaller, sub- In contrastto the situation for males,life span ordinate female in winter competitionfor food. appearedto be slightly greater for heavy fe- Observationsof pairs at feeding stationswould males. Regardlessof female weight, females indicate if the status of a bird's mate affected mated to light males had greater survivorship individual energy budgets at winter food than females mated to heavy males, although sources.However, it is alsopossible that males the effect of the mate is not as pronounced on matedto heavyfemales live longerbecause they females as on males. are higher quality males themselvesand also The light-heavy pairs did not appearto rear have accessto the preferred,heavy females.That moreyoung than other pairs(Marzluff and Bal- is, a male's survivorship may be independent da 1988b), but their sons (data are not available of the characteristics of his mate. for daughtersbecause of female-biasedemigra- Unlike males, heavy females and females tion, Marzluff and Balda1989) apparentlypro- matedto light malessurvived slightly better. It duced more sons themselves (Table 1). The cor- is not entirely clear how light males could en- relationbetween differences in parentalweights hance their mates' survivorship. The mate- (male-female) and the fecundity of their sons choice experimentsdid not show small males is negative and significantfor all pair types (r to be preferred (only that they were not dis- = -0.41, P = 0.05, n = 17). Weight differences criminated against). Thus we cannot attribute betweenparents were negativelycorrelated with the enhanced survival of females mated to small sons' lifespans (Marzluff and Balda 1988b). malesto the fact that thosequality femaleshad Therefore, the pairs with the smallestweight access to better males. differences,the light-heavy pairs, had greater There may be an optimal body size, some- longevitythemselves and had sonswith higher where between the average for males and fe- fecunditiesand greater survivorship. males, that maximizes autumn or winter survival in PinyonJays. Very smallbirds may not DISCUSSION be able to store sufficient fat reserves, whereas very large birds may require larger absolute The mate-choiceexperiments suggest that the amountsto survive. Large femalesand small ideal Pinyon Jay pair would be composedof a males would most closely approach this opti- brightly coloredmale, not particularlylarge or mum. necessarilydominant, paired to a large, aggres- Differential allocation of reproductive effort sive female with a thick bill. If Pinyon Jays is relevant to the questionof functional mate choosemates on the basisof geneticor parental choicefor body size. Pinyon Jaysmay allocate quality, pairs with these traits should have reproductiveeffort to maximize either self-sur- greater reproductivesuccess, survivorship, or vivorship or pair-survivorship (Burley 1985, both, than pairs with other attributes(for a dis- 1986).For example,in a specieswith long-term cussionof the possibleimplications of prefer- pair bondsin which survivalgreatly affects life- 302 JOHNSONAI-JD MARZLUFF [Auk, Vol. 107 time reproductive success,a high-quality bird conductcontrolled mate-choice trials using birds paired with another high-quality bird may at- of knownages. We expectthat suchtrials would tempt to maximize the survivorship of both reveal a type preferencefor experiencedindi- partners.A high-qualityindividual pairedwith viduals,although jays may activelyavoid pre- a low-quality bird may instead opt to extractas viously unsuccessfulbirds, regardlessof their much parentalinvestment as possiblefrom the experience(Marzluff and Balda1988a). poorer quality mate and hope to outlive it. In This is the first attempt we know of to un- the caseof Pinyon Jays,members of a pair are derstand avian mate choice by combining con- more likely than expectedby chanceto have trolled laboratoryexperiments with long-term similarsurvivorship (Marzluff and Balda1988a). field data. Our approachenabled us to circum- This is consistentwith the hypothesisthat they vent several of the methodologicalproblems allocatereproductive effort so as to maximize mentionedin the first sectionof the paper.Lab- pair survivorship, assuming that disappear- oratorymate-choice experiments have allowed ances of "widowed" birds are due to death, rath- usto identifypreferences for morphologicaland er than dispersal.Regardless of which of the color traits. Nonrandom mate choice with re- above strategiesbirds use, allocation of repro- spectto thesetraits occurs in the laboratory.We ductiveeffort on the basisof matequality could have found type preferencefor body weight in mean that survivorshipis a resultof a bird's the laboratorywithout assortativemating in the desirability as a mate, and not the reverse.If field and assortativemating for age in the field researchersuse survivorship to define mate that probablyindicates type preference. quality, but birds allocate reproductiveeffort Comparisonof the resultsof mate-choiceex- such that desirability affectssurvivorship, cir- perimentsand dataon maledominance showed cularity results. By using mate-choiceexperi- that male dominance does not override or mask ments to define quality, it is possibleto avoid female choice.It alsoappeared that female and this problem. male choiceoperated simultaneously. We have Light-heavy pairs had sonswith higher fe- avoidedthe complicationof territory quality by cundities and greater survival. It is troubling choosinga speciesthat doesnot defend a ter- that these light-heavy pairs do not appear to ritory. producemore sons than other pairs(we assume We have attempted to determine whether this meansthat they produce fewer offspring bodysize is a functionaltrait (i.e.whether males altogether). The possibility that Pinyon Jays gain by matingwith heavyfemales). Although might biassex ratios based on parentalweights the data suggestthat there may be a survival is intriguing. If so, heavy-heavypairs should advantageto malesmated to heavy females,it producemore daughtersand light-light pairs is not clear whether that advantageis actually more sons, but we cannot test this prediction conferred by the male's mate or is a quality with our data. intrinsic to the male himself. Wild Pinyon Jaysdo not mate assortatively We have not attemptedto determinewhether with respectto weight (Marzluff and Balda feathercolor, important in femalechoice, is an 1988b),probably because other traits not cor- aesthetic or functional trait. To look for a re- relatedwith weightare also important in•iica- lationship between reproductive successand tors of mate quality. However, Pinyon Jaysdo feather color would involve further fieldwork. appearto mateassortatively with respectto age Laboratoryexperiments using artificial aesthet- (Marzluff and Balda1988b). This pattern could ic markers(Burley 1986) would also be neces- occurby positive assortativemating with re- saryto determinepotential for mate choicefor spectto age.Alternatively, a preferenceby both aesthetic traits. sexesfor older, more experiencedindividuals Although we have learned much about Pin- could result in older, more desirable birds mat- yon Jaymate choice, there are still many gaps ing with one another,and so on (Burley 1983, in our understanding.One difficultywith com- Reid 1988).With very stablepairs, even random bining resultsof two separatestudies is that we matingcan resultin age correlationsbetween choseto investigatedifferent traits. If the ex- partners(Reid 1988).However, the randomiza- perimentshad been conducted before the field- tion procedureused by Marzluff and Balda work, featherbrightness could have been mea- (1988b) eliminates this as a possibility in the sured in the field and related to reproductive caseof PinyonJays. The bestway to distinguish histories. amongthe first two possibilitieswould be to Samplesizes for lifetimereproductive success April 1990] AvianMate Choice 303 are small, as with many long-term studies.This selection: testing the alternatives. Chichester, is perhaps the most difficult aspectof an inves- Wiley. tigation of functional mate choice. However, BRODSKY,L.M. 1988. Ornament size influences mat- for ornithologistswho have suchdata available, ing successin male Rock Ptarmigan. Anim. Be- hav. 36: 662-667. they may be combined with choiceexperiments BURLEY,N. 1977. Parental investment, mate choiceß to offer potentially important insights. and mate quality. Proc. Natl. Acad. Sci. U.S. 74: Clearly, the study of avian mate choice is 3476-3479. complicatedand requires careful thought and 1981a. Mate selectionby multiple criteria in planning. Our hope is that other researchers a monogamousspecies. Am. Nat. 117: 515-528. who study birds will profit from the successes, 1981b. Sexratio manipulation and selection as well as the shortcomings,of this study. for attractiveness. Science 211: 721-722. 1983. The meaning of assortativemating. Ethol. Sociobiol. 4: 191-203. ACKNOWLEDGMENTS 1985. The organizationof behavior and the evolution of sexuallyselected traits. Pp. 22-44 in This work was supportedin part by the Chapman Avian monogamy 8 (P. A. Gowaty and D. W. Fund, Sigma Xi, the University of New Mexico Stu- Mockß Eds.). Washington, D.C., Am. Ornithol. dent ResearchAllocations Committeeß the University Union, Ornithol. Monogr. 38. of New Mexico Biology Graduate Student Associa- --. 1986. Sexual selection for aesthetic traits in tion, and Northern Arizona University. R. Harris and specieswith biparental care. Am. Nat. 127: 415- G. Bell gave statisticaladvice. We wish to thank the 445. many people who assistedin various phases of the CATCHPOLE, C., B. LEISLER, & H. WINKLER. 1985. researchßespecially J. McConachie, R. Hutchins, D. Polygynyin the GreatReed Warblerß Acrocephalus Ligon, G. Foster,R. Balda,K. Bartlett,B. Burding,J. arundinaceus:a possible case of deception. Behav. Burding,and C. Marzluff. N. Burley,S. Lenington,J. Ecol. Sociobiol. 16: 285-291. LightbodyßR. Thornhillßand an anonymousreviewer COOKE,F., & J. C. DAVIES. 1983. Assortativemating, gave helpful comments. mate choice, and reproductive fitness in Snow Geese. Pp. 279-295 in Mate choice (P. Batesonß

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