The Auk 109(3):637-642, 1992

SELECTION OF BILL SIZE PROPORTIONS IN THE COMMON (CARPODACUS ERYTHRINUS)

MATS BJ•RKLUND Departmentof Zoology,Uppsala University, Box 561, S-75122 Uppsala,

ABSTRACT.--Thisstudy analyzedthe multivariatemorphological differences between sur- vivors and nonsurvivorsover winter in three years in the Common Rosefinch(Carpodacus erythrinus).In addition to the standardselection techniques commonly used, a number of multivariate analyseswere employed.Differential survival could not be accountedfor by differences in trait means. The variance-covariance matrices of survivors and nonsurvivors were highly significantlydifferent, indicating differences in characterrelationships between the groups.A principal-componentsanalysis of eachmatrix revealed that charactercorrela- tions on the first vector from each matrix differed. Among survivorsall characterswere positivelycorrelated to the firstvector, whereas among nonsurvivors the firstvector described bill width in relation to bill length. Therefore,these two characterswere chosenand used in a full-quadraticregression model. This analysisshowed a positiverelationship between survivaland the combinationof bill length and bill width, resultingin increasedvariance in bill width. In particular,survivors were characterizedby a positiverelationship between bill lengthand bill width, whereasnonsurvivors were characterizedby eithertoo broad,or too narrow a bill in relation to bill length. Possiblecauses behind this variation in bill proportionsmay be recently altered selectionpressures as a consequenceof a new habitat, and/or the particularconditions encountered during ontogeny(a purely environmental effect).Received 13 June1991, accepted 19 February1992.

PHENOTYPESDIFFER in survival and reproduc- among parts of the phenotype,and the rela- tion as a result of their properties (selection) tionship of phenotypeswith the environment and by chance (Sober 1984). This differential (Endler 1986, Mitchell-Olds and Shaw 1987, survival can result in evolutionary change in 1990, Wade and Kalisz 1990). charactersdepending on their geneticvariance An analysisof the sortingprocess can be per- and covariance with other characters(Lande formed in two basicallydifferent ways. First, 1976, 1979, Lande and Arnold 1983). Differen- one can use the standardprocedure to analyze tial survivalcan be studiedin two differentways the occurrence of selection of character means (Crespiand Bookstein1989, Crespi 1990):(1) in and resulting changesin variance (Lande and termsof the sortingprocess as such (Vrba 1989) Arnold 1983, Arnold and Wade 1984). Second, to see whether differential survival is a result a searchcan be made for differencesin phe- of the propertiesof the phenotypes(i.e. selec- notypic appearance between survivors and tion), or whether it is only a chanceprocess with nonsurvivorsby analyzingthe phenotypicvari- regard to phenotypic appearance;and (2) in ance-covariance patterns among these two terms of the evolutionary results of selection groups to see whether particular trait combi- (i.e. changes in character means over time as nations are related to differences in survival the result of selection; Lande and Arnold 1983, (Landeand Arnold 1983, Phillips and Arnold Arnold and Wade 1984, Endler 1986). 1989). If the phenotypeacts as an integrated Despite our limited knowledge of genetic whole, partitioning into different traits is more variancesand covariancesin natural popula- or less arbitrary (Gould and Lewontin, 1979), tions, numerousstudies of the possibleevolu- and multivariate assessment of differences tionary effectsof selectionhave been done dur- among groups is necessary. ing the last decade(see Endler 1986), while less In this paper, I will use these methods to attentionhas been devotedto the sortingpro- analyze three yearsof overwinter-survival data cess itself. This is unfortunate because a thor- in the migratory carduelinefinch, the Common ough comparativeanalysis of the propertiesof Rosefinch(Carpodacus erythrinus). Since adult the surviving and nonsurviving individuals,re- male mortality each year is about 50% (Bj6rk- spectively,can give insight into the properties lund 1989a),there is ample opportunityfor se- of phenotypes,the functional relationships lection.Since nothing is known aboutgenetic 637 638 MATSBJ6RKLUND [Auk,Vol. 109

variances and covariances of characters in this tive) wasanalyzed by comparingvariances before and species,the selectionanalysis will be restricted after selectionwhile correctingfor changesin vari- to methodsfor the detectionof phenotypiccor- ance due to possibledirectional selection (see Endler relates of differential survival in adult male 1986). Common . Second,to analyzepossible seiection on character combinations,I testedthe homogeneityof covariance matricesby a modifiedlikelihood-ratio statistic (Muir- METHODS head 1982). In the caseof only two matrices (as in this study), this test is a uniformly most-powerful The field work was carried out in R•ittvik, Central unbiased'test(Muirhead 1982). The test is available Sweden(60ø52'N, 1506'E) from 1985through 1988. For in the SAS (1985)statistical package in the DISCRIM a detaileddescription of the speciesand the study procedure.If a comparisonof survivorsand nonsur- area, see Bjfrklund (1989b). (malesonly) were vivors reveals that their covariance matrices are het- caught in mist nets upon arrival, measured,and in- erogeneous,then there is a possibilitythat they differ dividuallybanded. The followingmeasurements were in charactercovariances (probability of survival is taken:wing length(flattened); tail length;tarsus length not directly relatedto absolutesize of a character,but (measured as the distance between the extreme bend- to its size in relation to other characters). ing points at the intertarsaljoint and the toes);bill Third, I performeda principal-componentsanalysis length (from tip of the uppermandible to an inflexion on the survivor and the nonsurvivor groups,respec- point just behind the nostrils);bill depth; and bill tively, to see which charactersand charactercombi- width (this and previous charactermeasured at the nations differ between the groupsand if some char- front of the nostrils).Body masswas not used since acterswere redundantin the analysis.To analyzehow it is known to change considerably even within a many factors,or principal components,contain im- breeding season(Stjernberg 1979). Males have a high portant information the following approachwas used site fidelity between years (Stjernberg1979, Bjfrk- (adopted from Muirhead 1982:406-420).One wants lund 1990), and their rates of disappearance(ca. 50%) to find which, k, largesteigenvalues are distinct (bi- are very closeto thosefor other similar-sizedEuro- ologically relevant) among the total number, t, of pean species(Dobson 1987). Therefore, I am confident eigenvalues.This is a sequentialtest using the vari- that the main causeof disappearancefrom one year ance-covariance matrix, where the t - 1, t - 2 ... to the next was mortality rather than dispersal.Al- eigenvaluesare tested until we find the number of though numerousnestlings (ca. 150) were banded smallesteigenvalues that are equal and negligible, q overthe years,none of thesebecame part of the breed- = t - k. For details the reader is referred to Muirhead ing population.This meansthat the breeding popu- (1982). lation consists of birds born elsewhere. All males used Fourth, to searchfor possibleselection on character in the analysissang in the areauntil theywere paired, combinations,a full quadraticregression would have at which time some males moved out to breed some- been appropriate (e.g. Lande and Arnold 1983, Phil- where else(Bjfrklund 1990).Thus, there is a very little lips and Arnold 1989).However, to be able to do such chancethat some males were migrants on their way an analysis,the samplesize needsto be considerably elsewhere. I define survivors as males that were band- larger than the number of characters,preferably ed in one year and were seenin the area the next, greater than 100. Therefore, I used the results ob- whereas nonsurvivors were males that were not seen tained in the principal-componentsanalysis to reduce in a later year. This allows for pooling the data over the number of characters to be able to run the full the years,since each male only occursonce in the regressionmodel. The regressionon the remaining analysis. characters provides information on the directional To evaluate multivariate differences between sur- selectiongradient,/5•, and the quadraticselection gra- vivors and nonsurvivors, several methods were used. dient (stabilizing versusdisruptive selection),3'•, for All characterswere transformed by natural loga- characterz•, as well as the quadraticselection gradi- rithms. Each characterfor each group was tested for ents for the combinationof charactersz• and z•, % normalityusing Shapiro-Wilk's test (Shapiro and Wilk (Lande and Arnold 1983, Phillips and Arnold 1989). 1965). In no casedid the distribution differ signifi- I testedthe significanceof the predictorvalues in the cantly from normal. First, I performeda standardse- quadraticregression model by a likelihood-ratio test lectionanalysis to estimatethe occurrenceof selection following Johnson and Wichern (1988:288-289). In on charactermeans and variances(Lande and Arnold short, the model was fitted with and without one of 1983)using characters standardized to zero meanand the predictors.The improvement in the residualsum unit variance. Selection gradients (i.e. selection on of squareswas compared to the residualsum of squares character means after the effect of correlated char- for the full model. This gives an F-value with 1 (if acters has been removed) were estimated through only one predictoris deleted at the time) and n - r multiple regressionof survival on characters.Selec- - 1 degrees of freedom, where r is the number of tion on charactervariance (i.e. stabilizing or disrup- predictors, and n is sample size. July 1992] Selectionon Bill Size 639

T^BI•E1. Selectiondifferentials (i), selectiongradi- TABLE2. Correlations of characterswith first prin- ents (/•), and varianceselection coefficients (j) for cipal componentfor surviving and nonsurviving survival in male Common Rose . Critical val- male Common Rose finches. ues are Bonnferroni a00slevels (*, P < 0.05). Character Survivors Nonsurvivors Character ia /• fo Wing length 0.03 -0.19 Wing length -0.25 -0.17 -0.14 Tail length 0.70 -0.28 Tail length -0.01 0.08 0.08 Tarsuslength 0.31 - 0.40 Tarsuslength 0.14 0.13 0.49* Bill length 0.61 -0.88 Bill length -0.10 -0.10 -0.14 Bill width 0.95 0.70 Bill width 0.07 0.05 0.69* Bill depth 0.47 -0.07 Bill depth -0.21 -0.14 -0.19 n 29 35 Critical value +0.64 +0.59 +0.47

• Selectiondifferential standardized by SD of relativefitness. bStandardized by SD of relative fitnessand correctedfor effectsof directional selection. vector in the survivor group was biologically relevant, the comparisonbetween the groups was confined to this first vector. The first vectors Crespiand Bookstein(1989) suggested an alterna- of the two matricesdiffered widely in their tive methodwhere a generalsize vectoris assumed characterloadings, with a vector correlation (rv) and the selection coefficients for characters are the of only 0.13, which correspondsto an angle of differencesin adjustedmeans in an analysisof co- variance of the characters and survival with size as 82.5ø . In the survivor group all traits were pos- the covariate.In additionto the assumptionof a gen- itively correlatedto the first vector, indicating eral size factor, this method also assumes common a general size vector, but in the nonsurvivors slopesfor survivorsand nonsurvivors. In my dataset, group the first vectorwas dominatedby a high severalslopes in fact differed.Therefore, this ap- positive correlation with bill width, and an even proach was not used. higher negative correlation with bill length (Table 2). Since these two characters were the RESULTS only ones that were consistentlyhighly corre- latedin both groups,the following analysiswill In total, 29 surviving males and 35 nonsur- be confined to these characters. viving maleswere usedin the analysis.Selec- To assesspossible selection on covariation tion coefficientsas well as gradients(Table 1) among bill length and width, a full quadratic mostoften were far from being significant(all regressionwas performed on these two char- valuesP > 0.1), especiallywhen a tablewide a acters. This included absolute deviations from is employed (Rice 1989)of 0.05/6 = 0.008(Table charactermeans (fii), squareddeviations (•i), and 1). Thus, there was no detectable selection for cross-productsof the absolutedeviations for the changesin mean values for the measuredchar- two characters(•ii). This kind of analysisis best acters.Similarly, changesin charactervariances suitedfor large samplesizes. When samplesare were very low; therefore, further testing was small, as in this case, addition of single indi- not performed.Hence, there was no detectable viduals may have large effectson the results. stabilizingselection of any of the characters. This was dealt with in two ways.First, I checked The covariance matrices for survivors and the possible occurrence of outliers; an outlier nonsurvivorsdiffered significantly (X 2 = 140.22, was defined as having a residual value more P < 0.0001). This means that survival was re- lated to differences in the covariances of traits, TABLE3. Jackknifedestimates of quadraticselection sinceno significantdifferences in varianceswere coefficientsyielding estimatesof selection gradi- found (Table1). For survivors,only one vector ents (fi), stabilizing/disruptive selection (C,•),and selectionon charactercombinations (%), on sur- was unique, whereasthe other five were equal vival in male Common Rosefinches. (equality of the five smallesteigenvalues; X 2 = 31.11, P = 0.054); for nonsurvivors two vectors Bill character fi C •, P were distinct (equality of the four smallestei- Length 0.05 0.72 genvalues;X 2 = 21.22, P = 0.4). Among survi- Width 0.12 0.35 vors the first vector accounted for about 55% of Length 0.03 0.83 the total variance (Table 2), and for nonsurvi- Width 0.32 0.023 Length x width 0.34 0.024 vors only 37.6%(Table 2). Since only the first 640 MATSBJ•RKLUND [Auk, Vol. 109

2.00 meansamong individuals but to differencesin A Survivors 1.95 proportions between characters. Specifically, probability of survival was related to the rela- 1.90 tionship between bill length and bill width.

1.85 Relationshipsbetween bill morphologyand fitness have been demonstrated in several seed- 1.80 eating birds. This is particularly the case for

1.75 Galapagosfinches, where it hasrepeatedly been shown that food and morphology are causally 1.70 related (for review, see Grant 1986; Grant and 2.25 2.30 2.35 2.40 2.45 2.50 Grant 1989), but also is true for other finches 2.00 B Nonsurvivors (Schluter and Smith 1986, Smith 1990). Unfor- 1.95 tunately, nothing is known of the food of the Common Rosefinch in its winter quarters 1.90 (Bozhko 1980). Therefore, little can be conclud- 1.85 ed about the causes of natural selection in the Common Rosefinch--only that for the bill to 1.80 function optimally, bill length and bill width 1.75 are related to one another in a certain manner.

1.70 This meansthat for bill length a wide range of 2.25 values is possible provided the bill width has Bill I•ngth an appropriate value, and vice versa. Conse- quently, selectionon charactermeans in any Fig. 1. Regressionof bill width on bill length for directionis not to be expectedand indeed may (A) surviving and (B) nonsurviving male Common Rosefinches. be constrainedthrough the effectsof the other characters and combinations (Burger 1986, Wagner 1988).If this pattern of selectionis com- than +2 SDs from the mean. One individual mon and selection for the break-up of covari- was found outside that range and was deleted ation in bill design is rare, it becomeseasier to from the analysis. Second, I calculated a jack- understand why phenotypeswithin a given knife estimateof the regressioncoefficient by taxon--for example, cardueline finches--ex- deleting six individuals (randomly drawn) from hibit such a low level of phenotypic variation the data set and calculatingnew regressionco- in relation to the enormous time since diver- efficients. This was repeated 10 times. The re- gence (Bj•rklund 1991). suits presented in Table 3 are the jackknifed Differences in variance-covariance structure estimatesof the regressioncoefficients. Appar- amongsurviving and nonsurviving individuals ently, the resultswere robustagainst addition canbe expected,for example,when populations and deletion of individuals. The quadratic re- enter new habitats (Endlet 1986), a phenome- gressionmodel revealed a significant positive non that has been demonstrated (Service and selection on the character combination (F],55= Rose1985). The Common Rosefinchhas rapidly 6.36, P = 0.024; Table 3) and, as a result, an spreadwestwards in Europeduring the last de- increase in the variance in bill width (F],55= cades,entering many new areas and habitats 6.85, P = 0.023). In particular,surviving males (Bozhko 1980, Stjemberg 1985). Although rel- were characterized by a positive allometric re- evant datato a large extentare lacking,the find- lationship between bill width and bill length, ings in this study are at least compatiblewith whereas nonsurviving males generally had ei- the idea of environmentalchange as a causeof ther smaller or larger bill width in relation to changesand variation in the variance-covari- their bill length comparedwith the survivors ance structure of populations. (Fig. 1). An alternative explanation may be that in- dividuals differ as a result of different condi-

DISCUSSION tions during ontogeny.It has been repeatedly demonstratedthat differences,for example, in My resultsshow that the probability of sur- food composition and weather factors can vival was not related to differences in character strongly affect general body size and the size July1992] SelectiononBill Size 641 of different characters(e.g. James1983, Murphy related to a male-biased sex ratio? Anim. 1985, Boag 1987, Richner 1989, Alatalo et al. Behav. 38:1083-1085. 1990, Larsson and Forslund 1991). Nonsurviv- BJ•RKLUND,M. 1989b. Microgeographicvariation in ing individuals to a greater extent may have the song of the Scarlet RosefinchCarpodacus er- ythrinus.Ornis Scand. 20:255-264. sufferedfrom suboptimalconditions as young, BJ•RKLUND,M. 1990. Mate choice is not important eitherby purechance, or asa resultof genotype- for female reproductivesuccess in the Common environment interactions. In that case one Rosefinch(Carpodacus erythrinus). Auk 107:35-44. would not necessarilysee any selectionof trait BJ•RKLUND,M. 1991. Patterns of morphological correlationssince the origin of the variancethat variationamong cardueline finches (Fringillidae: selectionhas acted upon is not genetic. This ). Biol. J. Linn. Soc. 43:239-248. meansthat the phenotypic variance-covariance BOAG,P.T. 1987. Effectsof nestling diet on growth matrix may be a poor estimateof the genetic and adult size of Zebra Finches(Poephila guttata). variance-covariance matrix, and then selection Auk 104:155-166. coefficientsmay be poor predictorsof future BOZHKO,S.I. 1980. DerKarmingimpel. NeueBrehm- Bi•cherei 529, A. Ziemsen Verlag Wittenberg evolution (Endler 1986, Mitchell-Olds and Shaw Lutherstadt, DDR. 1987, Willis et al. 1991). BURGER,R. 1986. Constraints for the evolution of Finally, since the causesof change in char- functionally coupled characters:A nonlinear acter means are the differential reproduction analysis of a phenotypic model. Evolution 40: and survival of phenotypes(and not charac- 182-193. ters), only a thorough study of phenotypic CRESPI,B.J. 1990. Measuring the effect of natural propertiesincluding character combinations can selectionon phenotypicvariation on phenotypic give insight into why phenotypeschange or do interacting systems.Am. Nat. 135:32-47. not. Nonsignificant selection coefficientsin a CRESPI,B. J., AND F. L. BOOKSTEIN.1989. A path- standardmultivariate selectionanalysis do not analytical model for the measurementof selec- tion on morphology. Evolution 43:18-28. prove that individualsdo not differ in survival DOBSON,A. P. 1987. A comparisonof seasonaland probabilityas a result of their phenotypicap- annual mortality for both sexesof fifteen species pearance,only that: there is no selectionfor a of common British birds. Ornis Scand. 18:122- changein the mean of the measuredcharacter; 128. such selection is too weak to be detected; se- ENDLER,J. g. 1986. Natural selection in the wild. lection acts on combinations of characters; or Princeton Univ. Press,Princeton, New Jersey. we havebeen unable to properlyidentify what GOULD,S. J., AND R. C. LEWONTIN.1979. The Span- constitutes a relevant character. drels of San Marco and the Panglossianpara- digm:A critique of the adaptationistprogramme. Proc. Royal. Soc.Lond. B 205:581-598. ACKNOWLEDGMENTS GR•NT, B. R., AND P. R. GR•NT. 1989. Natural selec- I thank TorbjSrnFagerstrSm, Anders Forsman,Rus- tion in a population of Darwin's finches. Am. Nat. 133:377-393. sell Lande, Juha Meril• and Staffan Ulfstrand for valu- able discussionson this topic,as well as JonArnold, GRANT,P. R. 1986. Ecologyand evolution of Dar- SteveArnold and John Endlet for invaluable and con- win's finches. Princeton Univ. Press, Princeton, structive comments on previous versions of the New Jersey. manuscript.The work was madepossible by grants JAMES,F.C. 1983. 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