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Zonotrichia, Melospiza, Junco , and Passerella

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Zonotrichia, Melospiza, Junco , and Passerella PATTERNS OF GENIC AND MORPHOLOGIC VARIATION AMONG SPARROWS IN THE GENERA ZONOTRICHIA, MELOSPIZA, JUNCO , AND PASSERELLA ROBERT M. ZtNK Museumof VertebrateZoology and Departmentof Zoology,University of California, Berkeley,California 94720 USA ABSTRACT.--Analysesof genic variation and skeletal morphology were used to examine relationshipsamong 10 speciesin the generaZonotrichia, Junco, Melospiza, and Passerella. Cluster and principal componentsanalyses showed that morphologic differentiation in- volves size and aspectsof the skull, synsacrum,and hind limb. The genera have basically different skeletalmorphologies; there is someoverlap, however. The pheneticgroupings of taxa, based on skeletal morphology, were congruent with neither traditional taxonomic limits nor the geneticanalysis. The pheneticgroupings seem biased by nondivergenceand convergence.I conclude that the analysisof the genicdata producesa better estimateof the phylogenetichistory of the group than the analysisof morphology. The genic data show that the generaare distinctlineages, although the affinitiesof Z. capensisneed clarification.The branchingorder of Zonotrichia,J. hyemalis,and Melospizais unresolved,while P. iliacais probablya sistertaxon to thesethree genera.Melospiza melodia and P. iliaca are not dosely related, contraryto previous suggestions.The Lincoln'sSparrow and Swamp Sparrow are more similar to each other than either is to the Song Sparrow. Within Zonotrichia,the phylogenetichypothesis suggeststhat the White-crowned Sparrow and Golden-crownedSparrow are the most similar species,with the remaining taxa joining them in the following order:Harris' Sparrow,White-throated Sparrow, and Rufous-collared Sparrow. This phylogeneticscheme contradicts previous opinions, which, I suggest,were based on inconclusive evidence. The Harris' Sparrow, which is divergent relative to its congenersin both plumageand skeletalcharacters, is genicallysimilar to its congeners.The Rufous-collaredSparrow is morphologicallyand genicallydifferentiated from its north-tem- peratecongeners, and, if it is a valid member of Zonotrichia,it must be an early derivative. Heterozygosity(• = 0.039), percentagepolymorphic loci (,• = 20.3), and mean number of allelesper polymorphiclocus (• = 2.4) were similar to valuesreported for other birds and support the observationthat birds possesslevels of within-species geneticvariation typical of other vertebrates.However, geneticdistances averaged 0.06 between congenericspecies and 0.26 for noncongeneric(but confamilial)interspecific comparisons and are lower than those observedat comparabletaxonomic levels in other vertebrates.Rates of genic change seemhomogeneous. Converting genetic distances into estimatesof divergencedates sug- geststhat the generaoriginated from 1.3 to 6.6 MYBP. Speciationwithin Zonotrichiaand Melospizaprobably occurred in the Pleistocenebut before approximately140,000 yr ago. ! suggestthat Passerella,Melospiza, Junco, and Zonotrichiabe retainedas distinctgenera until comparablegenetic data from other emberizinesare available.Received 11 November1981, accepted26 March 1982. THE methodsof data gatheringand analysis (seeNevo 1978)and has provided, for example, used in systematicbiology have greatly ex- data on levels of genetic variation in natural panded in recent years. Biochemical assess- populations, on the genetic structure of pop- ments of genetic variation, quantitative anal- ulations and species,and on phylogenetic re- yses of genetic and morphologic data, and lationships among taxa. However, there have progressin the theoreticalaspects of system- been few quantitative multi-locus studies of aticshave provided powerful meansfor inves- proteinvariation at the specificand genericlevel tigating evolutionary relationshipsamong or- in birds (e.g. Barrowcloughand Corbin 1978; ganisms. The use of electrophoresisto study Avise et al. 1980a, b; Yang and Patton 1981) protein variationhas been especiallyprevalent relative to other vertebrate groups (Nevo 1978, 632 The Auk 99: 632-649. October 1982 October1982] EvolutionaryRelationships of Sparrows 633 Barrowclough 1980b). Similarly, there have ipers. The mean of the five measurementsfor each been relativelyfew phenetic(e.g. Schnell1970, characterwas computed for each taxon. While five Robins and Schnell 1971, Hellack and Schnell individuals cannot encompass within-taxon varia- 1977,Wood 1979)and cladistic(e.g. Payne and tion, it has been apparentlyassumed in other, sim- Risley 1976, Raikow 1976, Simpson and Cra- ilar studies(e.g. Schnell1970, Wood 1979)that such sample sizes are sufficient, because within-taxon craft 1981)appraisals of morphologicvariation variation is much less than among-taxonvariation. in birds. In few studies (Handford and Not- This assumption,in regardto geographicvariation, tebohm 1976) were protein and morphologic will be discussed below. variation examinedin concert.The increasing Principal componentsanalysis (PCA) and cluster use of thesetechniques and analyses,and more analyses(UPGMA and WPGMA) were usedto study than one data set, will be important to (1) eval- patternsof morphologicalvariation (seeSneath and uate evolutionary and systematicrelationships Sokal 1973). PCA is appropriatefor elucidating the among avian taxa, (2) compare avian evolution majorphenetic groupings of taxa.The principal com- at different levels(e.g. morphologicand genic), ponents, orthogonal and unrotated, were extracted and (3) generatedata that canbe comparedwith from a covariancematrix using the programPNCOMP (Duncan and Phillips 1980).The correlationsof char- resultsfrom other vertebrate groups. acterswith the first four componentswere examined The systematicrelationships among species to determine which characters best "summarized" in the generaZonotrichia, Junco, Melospiza, and the variation. Passerellahave been addressedby severalau- Becauseduster analysis is mostaccurate at the level thors (Linsdale1928; Dickerman 1961; Paynter of "branchtips" (i.e. higher levelsof similarity), it 1964, 1970; Short and Simon 1965; Mayr and is not suitablefor defining broadergroupings, the Short1970), but therehas been little recentsys- latter being sensitiveto different clusteringalgo- tematicwork on these taxa. In this paper I ana- rithms and distancecoefficients (Presch 1979; see be- lyze patterns of genic (= allozymic)and mor- yond). Therefore,ordination (e.g. PCA) and cluster- phologic(skeletal) variation in order to produce ing techniques are complementary and are both employedhere to evaluatethe morphologicdata set. independent,quantitative estimates of the sys- The raw character means were variance standard- tematic relationshipsand evolutionaryhistory ized, and the Taxonomic Distance (TD, Sneath and of these emberizine sparrows. Genic versus Soka11973)measure was used to constructan OTU x morphologicdifferentiation, rates and levels of OTU distance matrix (available from author). The genic divergence,and taxonomicrelationships program CLUST, written by W. W. Moss (Duncan are discussed. and Phillips 1980), was used to construct pheno- grams(for morphologicand geneticdata) and a PRIM METHODS AND MATERIALS (or minimum spanning)network. The clusteringand ordinationanalyses were used Morphology.--Taxa examined were: Rufous-col- on the 13-taxon x 40-character matrix. In addition, I lared Sparrow (Zonotrichiacapensis), White-crowned constructedphenograms from subsetsof the 13 taxa. Sparrow(Z. leucophrys),White-throated Sparrow (Z. This procedure involved the removal of one or two albicollis),Golden-crowned Sparrow (Z. atricapilla), subspeciesof P. iliaca in order to test whether mor- Harris' Sparrow (Z. querula), Song Sparrow (Melo- phologicallydifferent subspecies,when used in var- spizamelodia), Lincoln's Sparrow (M. lincolnii),Swamp ious combinations,resulted in different among- Sparrow(M. georgiana),Fox Sparrow (Passerella iliaca speciespattems. stephensi,P. i. canescens,P. i. townsendi),Dark-eyed Electrophoresis.--Samplesizes and generallocali- Junco (Juncohyemalis), and Bachman's Sparrow ties for specimensare given in Table 1. Samplesof (Aimophilaaestivalis); the latter taxonwas used as an liver, heart, and pectoralmuscle were storedat -76øC. outgroup. The subspeciesof P. iliaca were used as For preparation of tissue extracts, samples were separateOperational Taxonomic Units (OTU's) (see thawed, minced with a razor blade, and combined below). Specimensused in this study are housedat with an equal volume of deionized water. Samples the Museum of Vertebrate Zoology, University of were then centrifuged at 16,000 rpm for 40 min at California, Berkeley;further informationconcerning 4øC. The supematant was frozen at -76øC for later these specimensis available from the author. Five electrophoreticanalysis. skeletonsper taxon were measuredfor 40 characters ! examined39 presumptivegenetic loci (Appendix (described in Robins and Schnell 1971) from most 2) using standardstarch gel electrophoreticproce- bodyregions (see Appendix 1). Only adultmales were dures (Selander et al. 1971, Avise et al. 1980a, Bar- used exceptfor one female eachof Z. leucophrysand rowclough1980b, Yang and Patton1981). Protein as- Z. albicollisand two of M. georgiana.Measurements sayswere preparedfollowing Selander et al. (1971), were recorded to the nearest 0.05 mm with dial cal- Harris and Hopkinson (1976), and Yang and Patton 634 ROBERTM. Z•NK [Auk,Vol. 99 (1981). Further information on electrophoreticcon- the genera generally occupy different regions ditions is available from the author. of the 40-character
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