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 inter- est. 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