GENIC VARIATION, SYSTEMATIC, AND BIOGEOGRAPHIC RELATIONSHIPS OF SOME GALLIFORM BIRDS

R. J. GUTIERREZ,1 ROBERTM. ZINK, AND SUH Y. YANG2 Museumof VertebrateZoology, University of California,Berkeley, California 94720 USA

ABSTRACT.--Starchgel electrophoresiswas used to evaluate levels and patterns of genic differentiationamong 10 speciesof galliform birds in the Phasianidae(9) and Tetraonidae (1). The phasianidsincluded an Old World quail, a partridge, a pheasant,and six species of New World quail. Measuresof within-speciesgenetic variation includedheterozygosity, percentagepolymorphic loci, and number of allelesper polymorphiclocus. These values were similar to but lower than those reported for other birds. Genetic distancesamong conspecificpopulations and among congenericspecies were low comparedto other avian results. Genetic distancesamong noncongenersboth within and between families were considerablyhigher, however, than those reported for passerinebirds. Thus, more studies of levelsof genic differentiationamong nonpasserines are required to complementthe lit- erature on genic divergenceamong passerinesand to enable us to make general statements about genic evolution in birds. Phenogramsand phylogenetictrees suggestedthat Phasianuscolchicus, Tympanuchus pal- lidicinctus,Coturnix coturnix, Alectoris chukar, and the New World quail (Odontophorinae) are genically distinct taxa. The branching sequenceamong the non-Odontophorine taxa is unresolvedby our data. The branching order among taxa in the Odontophorinaefrom a commonancestor is: Cyrtonyxmontezumae, Oreortyx pictus, Colinus virginianus, Callipepla squamata,Lophortyx gambelii, and L. californicus.The generaCyrtonyx, Oreortyx, and Colinus are clearly distinct from Callipeplaand Lophortyx,which are quite similar to each other genically. We use a fossil speciesfrom the mid-Miocene of Nebraskato calibrateour geneticdis- tances.We estimatedates of divergenceof taxain the Odontophorinaeand offer a hypothesis on their historicalbiogeography. Our analysissuggests that three east-westrange disjunc- tions could accountfor the origin of Oreortyx (12.6 MYBP), Colinus(7.0 MYBP), and Calli- pepla-Lophortyx(2.8 MYBP). We suggestthat L. californicusand L. gambeliishould be con- sidereddistinct speciesbecause of an apparentlack of panmixia in zonesof sympatry,even though the D between them is typical of that found between subspeciesof other birds. Oreortyxand Colinusshould remain as distinct genera,while our data are equivocalon the statusof Callipeplaand Lophortyx?Received 9 March 1982, accepted5 July 1982.

ALLOZYMEelectrophoresis has been used less examinedavian intrafamilial relationships(e.g. frequently to examinegenetic variation within Barrowclough and Corbin 1978, Avise et al. and among groups of birds than in other ver- 1980a-c).They have found that passerinebirds tebrates (see review in Nevo 1978). Some possess considerably lower levels of genic workers have examined patterns of intraspe- (= allozymic) differentiation than other verte- cificgenic variation in passerines(e.g. Barrow- brate taxa, at comparable taxonomic levels. clough 1980,Johnson and Brown 1980, Corbin Several workers have compared the level of 1981, and references therein), and a few have genic divergence and taxonomicrank for var- ious vertebrate and invertebrate taxa (e.g. Ay- • Present address: Department of Wildlife Man- ala 1975, Avise et al. 1980b). Barrowcloughet agement, Humboldt State University, Arcata, Cali- fornia 95521 USA. al. (1981)present similar data for birds but dis- 2 Present address:Department of Biology, Inha cussreasons why comparisonsacross different University, Inchon, Korea. groups of organisms may be inappropriate; :3Lophortyx has been merged with Callipeplain the these include taxonomic artifacts [e.g. avian, Thirty-fourth Supplement to the American Orni- mammalian, and reptilian genera may not be thologists'Union check-listof North American Birds comparablebecause of the way in which tax- [Auk 99 (3, Suppl.): 5CC]. onomistspartition variation (Sibley and Ahl- 33 The Auk 100:33-47. January1983 34 GOX•gRREZ,ZINK, ANDYANG [Auk, Vol. 100

quist 1982)] and differences in rates of evolu- zygosity(/•) was definedas the numberof hetero- tion, mating systems,effective population sizes, zygous genotypesrecorded in a sample divided by recencyof common ancestry,and dispersalpa- the product of the number of loci and the number of rameters. Whether or not low levels of genic individualsassayed (see Corbin 1981for a discussion divergencetypify birds as a group is unclear, of calculating/z/).Estimates of percentagepolymor- becauseonly Barrowcloughet al. (1981)studied phismwere based on thenumber of locihaving more than one allele divided by the total number of loci a nonpasserinetaxon. They found higher levels (27) examined. of differentiation among some procellariiform The measuresof Nei (1978)and Rogers (1972) were taxa than those usually found among passer- used to estimate genetic distances between taxa. ines. Becausethe levelsof geneticdifferentia- Clusteranalyses, summarizing the matrixof Rogers' tion are sometimes used to make inferences D-values,were performed with boththe unweighted about evolutionaryprocesses (Avise et al. 1980c, and weighted pair-group methods,using arithmetic Templeton 1980), we clearly need additional means(UPGMA and WPGMA, respectively).The co- studies of nonpasserinesbefore we can make phenetic correlation coefficient, rcc,was used to eval- general statementsabout genic evolution in uate how well the resultant phenogramsrepresent birds. the original distancematrix. Sneathand Sokal(1973) provide details on these pheneticmethods. Phylo- The patternsof genic differencescan alsobe genetic trees, also based on Rogers'D-values, were used to infer phylogeneticrelationships (e.g. constructedaccording to the methodsof Farris (1972; Barrowcloughand Corbin 1978,Zink 1982). In Wagner trees) and Fitch and Margoliash(1967; F-M this paperwe examinelevels of genicvariation trees). The Wagner tree is an approximationof the and phylogenetic relationships among 10 most parsimonious tree. The F-M procedure con- speciesfrom 5 of 10 generaof New World quail, structsa number of treesby alteringthe branching an Old World quail, a partridge, a pheasant, structureand branch lengths. Alternative trees were and a grouse. We use our phylogenetic hy- evaluatedby the percentagestandard deviation (%SD) pothesis to construct an estimate of the evo- and by the numberof negativebranches (the fewer the better). A lower %SD means a better fit of dis- lutionary history of some New World quail. tancesimplied by the tree to the original distance We also evaluateprevious statementsabout the matrix (Fitch and Margoliash 1967). A cladisticanal- taxonomic relationships of these galliform ysis, sensuHennig (1966), using alleles as character birds. states (see Wake 1981), basically corroborated the above methods. The allele in T. pallidicinctus(Te- MATERIALS AND METHODS traonidae) was considered"primitive" when com- We examined 217 specimens of galliform birds paring the pattern of allele distribution in the re- representing 10 species. Species, localities, sample maining taxa (Phasianidae),i.e.T. pallidicinctuswas sizes, and the taxonomic framework used in this pa- used as an "outgroup" to the phasianids. per are given in Appendix 1. Nomenclaturefollows the A.O.U. check-list (1957, 1973). RESULTS Liver, heart, and kidney tissuewere excisedin the field within 4 h of death and frozen in liquid nitro- Protein variation.--Twenty structural pro- gen. Tissueswere homogenizedusing the methods teins and enzymes encodedby 27 presumptive of Selander et al. (1971), and extractswere stored at genetic loci were examined in all individuals. -76øC until used for electrophoresis.Combined tis- Allelic frequenciesfor the 23 variable loci, per- sue extractswere subjectedto horizontal starch gel centagepolymorphism and heterozygosity,and electrophoresisas describedby Selanderet al. (1971). number of alleles per polymorphic locus are Gel and buffer systemsfor the loci listed in Appendix given in Appendix 2. Four loci (Mdh-1, Mdh- 2 were essentiallythe same as those describedby Yang and Patton (1981). More detailed information 2, Lap, Pt-l) were monomorphicand fixed for regardingelectmphoretic conditions is availablefrom the same electromorph acrossspecies. Seven the authors. loci (c•Gpd-1,Got-2, Udh, Gdh, Ldh-1, Ldh-2, We assumethat our electrophoreticallydetectable Pept-2) were monomorphicwithin speciesbut variants (= electromorphs)at a locus differ geneti- exhibited interspecific differences. The re- cally; hence, we refer to them as alleles.Alleles at a maining loci were polymorphicin somespecies locus were coded by their mobility from the origin. and alsoshowed interspecific fixed differences. Thg most anodal allele was designated as a, with We excludethe laboratorystrains of Coturnix slower alleles denoted as b, c, d, etc. Isozyme no- and Alectorisfrom discussionsof within-species menclaturefollows Yang and Patton (1981). Hetero- variation, becausethese levels of variation may January1983] GenicVariation in Galliforms 35

TABLE1. Matrix of geneticdistances between 17 taxa of galliform birds. Distancescomputed by methods of Nei (1978) above diagonal and Rogers(1972) below diagonal.

Species Species I 2 3 4 5 6 7 1. Tympanuchuspallidicinctus -- 1.041 1.308 1.291 1.326 1.201 1.483 2. Phasianus colchicus 0.649 -- 1.446 1.282 1.310 1.172 1.654 3. Coturnix coturnix A 0.721 0.749 -- 0.064 0.059 1.185 1.340 4. C. coturnix B 0.713 0.714 0.109 -- 0.056 1.136 1.209 5. C. coturnix C 0.729 0.721 0.086 0.101 -- 1.190 1.346 6. Alectoris chukar 0.695 0.682 0.685 0.665 0.689 -- 0.962 7. Lophortyxgambelii 0.769 0.799 0.725 0.692 0.730 0.616 -- 8. L. californicusA 0.773 0.797 0.728 0.690 0.730 0.617 0.028 9. L. californicusB 0.774 0.801 0.732 0.694 0.734 0.617 0.032 10. L. californicusC 0.768 0.795 0.727 0.688 0.728 0.610 0.037 11. Callipeplasquamata A 0.773 0.758 0.752 0.727 0.761 0.652 0.106 12. C. squamataB 0.764 0.750 0.742 0.720 0.752 0.644 0.106 13. Colinusvirginianus A 0.770 0.732 0.741 0.741 0.753 0.687 0.262 14. C. virginianusB 0.772 0.729 0.739 0.738 0.751 0.687 0.262 15. Oreortyxpictus 0.808 0.764 0.751 0.744 0.760 0.649 0.348 16. Cyrtonyxmontezumae A 0.744 0.731 0.746 0.737 0.754 0.684 0.497 17. C. montezumae B 0.735 0.727 0.742 0.734 0.751 0.680 0.492

TABLE 1. Continued.

Species

8 9 10 11 12 13 14 15 16 17

1.495 1.495 1.475 1.493 1.476 1.487 1.495 1.668 1.364 1.335 1.627 1.646 1.617 1.430 1.419 1.342 1.331 1.476 1.334 1.326 1.340 1.343 1.330 1.448 1.429 1.393 1.389 1.450 1.416 1.407 1.204 1.216 1.192 1.339 1.345 1.423 1.413 1.433 1.399 1.390 1.327 1.335 1.312 1.467 1.449 1.427 1.421 1.468 1.435 1.425 0.967 0.966 0.947 1.071 1.054 1.184 1.189 1.056 1.170 1.158 0.005 0.007 0.008 0.089 0.082 0.295 0.295 0.410 0.671 0.653 -- 0.000 0.000 0.115 0.100 0.301 0.298 0.418 0.640 0.624 0.013 -- 0.000 0.121 0.102 0.306 0.304 0.421 0.634 0.617 0.019 0.015 -- 0.120 0.103 0.308 0.306 0.431 0.641 0.623 0.129 0.130 0.131 -- 0.003 0.258 0.262 0.491 0.664 0.645 0.125 0.117 0.126 0.022 -- 0.241 0.244 0.473 0.613 0.593 0.274 0.276 0.280 0.244 0.229 -- -0.002 0.538 0.478 0.462 0.273 0.277 0.283 0.252 0.237 0.015 -- 0.540 0.463 0.448 0.355 0.354 0.367 0.400 0.391 0.424 0.427 -- 0.746 0.744 0.479 0.476 0.479 0.493 0.473 0.395 0.385 0.533 -- 0.001 0.476 0.472 0.472 0.483 0.463 0.389 0.383 0.533 0.018 --

havebeen affectedby prolongedcaptivity. The ble 1. A summary (Table 2) of genetic distance averageproportion of polymorphic loci for the as a function of various taxonomic groupings wild speciesis 14.5% (range0-29.6%). F/ is showsthat /• increasesas taxonomicgroup- 2.6% and rangesfrom 0 to 5.1% (Appendix 2). ings become more inclusive, at least to the Thevalues of F/, percentagepolymorphic loci, subfamily level. This suggeststhat the taxo- and number of alleles per polymorphic locus nomic groupings are "biologically real," based are similar to but lower than thosereported for on our geneticanalysis. Levels of/• for other other groupsof birds (Barrowcloughand Cor- avian taxa are also shown in Table 2 for com- bin 1978, Avise et al. 1980a, Zink 1982). parisonwith the galliform/•'s. Interspecificgenetic distance.--The matrix of At the local population level, the galliforms genetic distancesbetween taxa is given in Ta- sampledhere showless differentiation (/• = 36 GOneRREZ,ZINK, AND YANG [Auk, Vol. 100

•. pallidicinctu$ P. colchicu$ •A t Coturni•coturnix A chukar œ. •ambeh'i ½I œ'califor- Bj nicu$

A0 1 Callipepla$quamata •B I Co#nu$vH•inianu$ O. pictus UPGMA r½½= .99 • I Cyrtonyxmontezumae I ß .8 Rogers' D

I I I I I .58.9 16.0 7.5 2.7 0 Million yeors Fig. 1. UPGMA phenogramderived from the matrix of Rogers'D-values (Table 1). Geographiclocalities given in Appendix 1. Time scaledetermined from the formula ! = 26.3 x 10"D; see text.

0.0007) than other birds, although this may be only slightlybelow the rangegiven by Barrow- due to the closeproximity of some of the sam- cloug_h,0.0078-0.1267, for congenericspecies. ples (Appendix1). The D-valuebetween L. The D between noncongenericspecies in the gambeliiand L. californicus,0.0067, is similarto Odontophorinae, 0.412, is considerablyless that observedbetween subspeciesof other birds thanthe D betweenthese and the other pha- [0.0048 + 0.0049(Barrowclough 1980)], but it is sianids, 1.32. Both of these values are greater

TABLE2. Mean geneticdistance (Nei 1978)as a function of taxonomicrank in somegalliform birds. Taxa includedin eachtaxonomic level are given in Appendix1. D-valuesfrom Table 1. Alsogiven are D-values at comparabletaxonomic levels for other birds (from Barrowclough1980).

Number of compari- Comparable data Taxonomiclevel sons /• -+ SD Range for otherbirds Local population 6 0.0007 -+ 0.0013 -0.00151 to'0.00331 0.0024 -+ 0.0028 Congeneric species(Lophortyx) 3 0.0067 -+ 0.0014 0.00507 to 0.00775 0.0440 _+ 0.0220 Noncongeneric speciesin Odontophorinae 46 0.4116 _+ 0.2021 0.0824 to 0.7460 0.2136 _+ 0.1659 Species in Odontopborinae vs. Phasianus colchicus, Coturnix coturnix, and Alectoris chukar 62 1.3210 _+ 0.1640 0.962 to 1.654 not available Tympanuchuspallidicinctus (Tetraonidae) vs. all other species(Phasianidae) 16 1.4000 _+ 0.1500 1.041 to 1.668 0.6829 •* _+ 0.1970 Basedon study by Barrowcloughet al. (1981)of someprocellariiform birds. January1983] GenicVariation in Galliforrns 37

F. pallidicinctu$ 5.20 t•. colchicus 5.29 .59 5.00 .47 A coturnix .2•/.54 GB tcoturn/x 3.00 ,4. chukar

.59

.64I 1•5 t. •ambe///

.65 ' Lø•B • squamata .o• .58 B vir•inianus 1.50 2.25 O. pictus WAGNER%S D = 9.19 2.46 .•4.•04 AiB montezumaCyrtony x Fig. 2. Wagner tree basedon Rogers'D-values. Branchlengths in units of Rogers'D (x10). The tree is "rooted" at T. pallidicinctus(Farris 1972).

than that given by Barrowclough(1980) for oth- shown (Fig. 1). The Wagner (Fig. 2) and F-M er avian cdnfamilialbut noncongenericcom- (Fig. 3) trees resembleFig. I in terms of the parisons(/• = 0.2136), suggestingthat the overall relationships suggested. Differences Odontophorinae is a distinct group. At the among these three analysessuggest to us that familylevel, the/• observedbetween T. palli- the branching sequence of the subfamilies, dicinctus(Tetraonidae) and the other species(all while themselvesgenically distinct in all anal- in Phasianidae), 1.400, is approximately twice yses, is unresolved by this analysis. That is, the/• reportedfor interfamilialcomparisons of we do not believe that a clearhypothesis of the other birds (0.6829). branching order of the subfamilies emerges Genic relationshipsamong species.--For two from our data. The level of differentiation and reasons,phenetic (UPGMA and WPGMA) and the branchingdiagrams show considerabledi- cladistic(Wagner and F-M) procedureswere vergence, at the structural gene level, among used to constructbranching diagrams (Figs. 1- thesegalliform birds. The branchingsequence 3). First, we wanted to determine whether or of taxa within the Odontophorinae was iden- not the branchingstructure was dependenton tical in all branching diagrams; therefore, we which methods were used (see Presch 1979). feel that it is a robust result. Second, the methods for constructingtrees, as The branching diagrams show that there is opposedto phenograms,are independentof considerabledivergence among taxa within the the assumptionof homogeneityof evolution- Ondontophorinae, and we now discuss rela- ary rates and, hence, provide estimatesof the tionships in that group. Given the patterns in amount of genic change along branches;Fel- Figs. 1-3, it seems unlikely that the level of senstein (1978) discussesthese assumptionsfor divergenceamong local populationswould be Wagner trees. sufficient to alter among-speciespatterns es- The UPGMA and WPGMA phenogramshad tablished here. Thus, we doubt that an analysis equal r,,.'s (0.99) and were topologicallysimi- of geographicvariation, not addressedhere, lar; therefore,only the UPGMA phenogramis would alter our conclusions, which follow. Lo- 38 GUTII2RREZ,ZI•C, A•D YA•O [Auk,Vol. 100

5 27 5 27 7• pall/•Y/c/nctu$ 522 $.22 -.01 .70{ F• colch/cu$ 2.94 •. chu•ar 302 .49

301 3•3 .•7C coturn/x 21.4•1•AB }Coturnl• ]L .11 A •

1.26

F-M

%SD= 5.76 Lneg • ] I •3 O.p/c/us z- M 254 .12A Cyrtonyx %SD = 7.29 2 negs

Fig. 3. Fitch-Margoliash(F-M) treesbased on Rogers'D-values. Branch lengths in Rogers'D (x10). These two trees,of fourexamined, best summarized the originalmatrix, as judged by thevalues of the percentage of standarddeviation and the numberof negativebranches. These trees, as well asthose in Figs.1 and 2, showthat alternativehypotheses exist regarding the branchingsequence of the five subfamilies. phortyx gambelii and L. californicus,the only Sibley and Ahlquist 1982, Avise et al. 1980c). congenersin our study, consistentlycluster to- We believe that the most reasonablecompari- gether--the only genetic differenceswe found sonsinvolve congeneric,interspecific levels of between them are minor gene frequency dif- differentiation, when comparingacross verte- ferences(Appendix 2). Lophortyxand Callipe- brate classes(Zink 1982). Avian specieslimits pla are the most similar pair of genera in our are usually clearly defined, whereas higher sample of Odontophorinae.The other genera taxonomiccategories are far more arbitrary, es- in the subfamily, Colinus,Oreortyx, and Cyr- pecially across vertebrate classes.Thus, it is tonyx, are each genically distinct, as evidenced important to note that passerinecongeners by the level of separationon phenogramsand show little genic differentiation. Research branch lengthson F-M and Wagner trees. At should address this problem rather than dif- aGpd-1, all members of the Odontophorinae ferencesbetween intergeneric or familial levels are fixed for the same, apparently derived al- of genic divergenceacross vertebrate classes. lele. Various groupsof taxa in the subfamily Unfortunately, our only congenericcompari- are fixed for alleles not found in any non- son, L. gambelii-L. californicus, is between Odontophorine taxon at Udh, Pept-1, Pept-2, probablesibling species. and Est-2. The relationshipsamong P. colchi- Within a major vertebrate classes,compari- cus, C. coturnix,C. virginianus,L. gambelii,and sons of equivalent taxonomiclevels above the L. californicusare similar to thosesuggested by species level may be more appropriate. The Jolleset al. (1979)based on lysozymesequence demonstration(Barrowclough and Corbin 1978, data. Barrowcloughet al. 1981,Zink 1982,this study) that avian genetic distances increase as the DISCUSSION taxonomic unit compared is more inclusive suggeststhat the taxonomichierarchy reflects Levels of genetic differentiation.--It is fairly biological, or phylogenetic, units. We found well established that genetic differentiation that, at the genericand family levels,the gal- among passerinetaxa is low relative to other liforms are considerably more differentiated vertebrates(Avise et al. 1980c,Barrowclough than passerinetaxa (Table 2). We clearly re- et al. 1981). The reasonsfor this are unclear (see quire more comparisonsof nonpasserinetaxa January1983] GenicVariation in Galliforms 39 before we will understand whether or not non- rived characterstates (synapomol'phies) sup- passerinespresent a differentpattern from that port the monophylyof the Odontophorinaeand of passerines.For example,the genetic dis- each of the two subgroups. tanceswe observedmay be amongthe highest Of interest here is Cyrtonyxcooki, an extinct found in nonpasserines,but this remainsto be speciesfrom the mid-Miocene [16 million yr documented. beforepresent (MYBP)] of Nebraska(Brodkorb Rates and datesof divergence.--Thebranch 1964)and a congenerof a speciesexamined by lengthsof the Wagner(Fig. 2) and F-M (Fig. 3) us (C. montezumae).We assume here that this treescan be interpretedas roughestimates of fossil belongs to the monophyletic lineage "rates"of genicdivergence, thereby indicating Cyrtonyx,and it is neitherfrom the Odontopho- lineagesthat havechanged faster or slowerrel- rine stockthat pre-datedthe Dendrortyx-Odon- ative to other lineages.Rates are averagesacross tophorussplit, nor is it a primitive (pleiso- loci. The branch lengths (rates)in Figs. 2 and morph) early member of the Dendrortyxgroup. 3 appearhomogeneous, although with missing Thus, the age of C. cooki can be taken as a extant taxa this is difficult to judge, because conservativeestimate of the age of the Cyrto- additional taxamight have evolvedat different nyx lineage, representedin our study by C. rates than the taxa we sampled.The branch montezumae.The averageof D-values from C. lengths (Fig. 2) from the "most recent common montezumaeto its sister taxa in the Odontoph- ancestor" to members of the Odontophorinae orinae (Fig. 1, Table.I), 0.609, is assumedto range from 2.29 (to C. squamata)to 2.83 (to ¸. representminimally 16 million yr (MY). This pictus),and the mean(+SD) equals2.59 + 0.17; resultsin the following conversion:t = 26.3 x thus, we suggestthat evidenceof rate hetero- 106D. We use this calibration to indicate pos- geneity is lacking among thesetaxa. sibledates of divergenceamong the taxa shown Nei's measure of genetic distance can be in Fig. 1. We stressthat this is a rough estimate converted into approximate dates of diver- (but probablyconservative), owing to the vari- gencebetween taxa (Nei 1975).Nei suggested anceof geneticdistances between taxa. It is the a "theoretical" conversion of t = 5 x 106D, first suchapproximation for an avian taxon. where t is time since divergencefrom a com- Holman (1961) discusseda fossil, Lophortyx mon ancestor, and D is Nei's D-value. Yang shotwelli,from Umatilla County, Oregon. This and Patton (1981) used this conversion to es- specimenis associatedwith mammalian re- timate divergence dates among Galapagos mains from the Hemphillian stage,dated at 6 finches.As Yang and Patton and Avise et al. MYBP (Savagepers. comm.). Holman noted that (1980c) noted, other attempts to calibrate this specimenpossessed several characters un- D-values (e.g. Sarich 1977) suggestthat Nei's like modem Lophortyx,and therefore its po- calibration may be low (i.e. too rapid) by a sition in the evolutionaryhistory of Callipepla factor of four. Workers with other vertebrate and Lophortyxis uncertain. If this fossil is a groups (e.g. Maxson and Maxson 1979) have "good" member of either Callipeplaor Lophor- used the fossil record and independent esti- tyx, it would greatlyalter our calibrationof ge- mates from microcomplementfixation studies netic distances. For instance, our estimated date to calibrate electrophoreticdistances and di- of the divergence of Callipeplaand Lophortyx, vergencetimes, and such studieshave tended 2.8 MYBP, would necessarilybe •>6 MYBP, or to supportSarich (1977). twice our presentestimate. Prager et al. (1974) The fossilrecord of the galliforrnsallows what suggestedthat phasianoidtransferrins evolved amountsto the first independentcalibration of at a rate of 0.97/MY. Prager and Wilson (1976) avian genetic distances.Several assumptions gave a transferrinimmunological distance of 65 are made in our calibration. First, based on our for P. colchicus-C.virginianus, or a divergence reading of Holman's (1961, 1964)extensive os- date of 63 MYBP. Our data (D = 1.34) suggest teologicalanalyses, we assumethat the Odon- a divergencedate of 35 MYBP. Unfortunately, tophorinaeis a monophyleticgroup consisting this is the only comparisonin common be- of two subgroups: the ¸dontophorus group tween our studyand Pragerand Wilson's(1976). (consistingof ¸dontophorus,Dactylortyx, Cyr- It is of interest that their estimate of the diver- tonyx, and Rhynchortyx)and the Dendrortyx gencedate for thesetwo taxais twice ours and group (containingDendrortyx, Philortyx, ¸re- in the same direction as our estimate would be ortyx, Colinus,Callipepla, and Lophortyx).De- if L. shotwelliwas a valid Lophortyx.Clearly, 40 GUTIERREZ,ZINK, AND YANG [Auk, Vol. 100

:•'::- Oreortyxp/•tu$ Lophort,vxcah'form•u$ :• Lophort,vx•arnbeh'/ :"'..:.::•Calh•epla squarnata • Colinu$wi•ianu$

Fig.4. Approximatebreeding distributions (excluding introductions) of Oreortyx pictus, Colinus virgin- ianus,Callipepla squamata, Lophortyx gambelii, and L. californicus.These species are all representatives of the subfamilyOdontophorinae. Ranges taken from Leopold et al. (1981). the discrepancyin our estimatesdeserves fu- middleOligocene of Colorado,and the lower ture attention, as does the phylogeneticposi- Miocene (approximately20 MYBP) of South tion of L. shotwelli. We conclude at this time Dakota(Brodkorb 1964). This suggestsa fairly that Nei's (1975)conversion factor given above widespreaddistribution of ancestralOdon- is probablylow by a factorof five for the gal- tophorinestock. Therefore we will applymeth- liforms studied here. We note also that many odsfrom vicarlance biogeography (Nelson and assumptions,such as phylogenetic hypotheses Platnick1981) to generateour biogeographic of fossil and recent forms, need to be tested. hypothesis.We assumefirst that the Dendror- Biogeographyof the Dendrortyx group of the tyx and Odontophorusgroups are distinct, Odontophorinae.--Asmentioned above, the monophyleticlineages (discussed above) that Dendrortyxgroup of the Odontophorinaecon- divergedat least16 MYBP(middle Miocene). sistsof the generaDendrortyx, Philortyx, Ore- Next, we assumethat Dendrortyxand Philortyx ortyx,Colinus, Callipepla, and Lophortyx.Al- are primitiveand/or have not affectedthe dis- thoughwe lackDendrortyx and Philortyx in our tribution of the remaining species. The re- geneticanalysis, we will usethe phylogeny of stricted distribution of Dendrortyx(M6xico to the remainingtaxa and our approximate dating Costa Rica) and Philortyx (M6xico) suggests of dadogeneticevents (Fig. 1) to developan relict status and, therefore, "primitiveness." evolutionaryperspective of the biogeography Based on their skeletal morphology, Holman of thesetaxa. Without an objectiveestimate of (1961) concluded that these two genera were phylogeneticrelationships, it wouldbe diffi- the mostprimitive members of the Dendrortyx cult to evaluate historical evolutionary patterns group. These assumptionsobviously need amongthese New Worldquail given simply a testing. mapof theircurrent distributions (Fig. 4). The remaining stepsin our biogeographic The earliestknown fossil Odontophorinae are hypothesisare outlined diagrammatically in Fig. fromthe earlyOligocene of Saskatchewan,the 5. Thegenetic data indicate that O. pictusorig- January1983] GenicVariation in GalIiforms 41

inated about 12.6 MYBP (Fig. 5a) and probably evolved in western North America, based on iii•0A. 12.6 MYBP/, '• its current distribution (Fig. 4). Perhapsdrying reortyx / 'pre'-' Coh•us- p/ctus / C•///•oep/•- Lophortyx trends at this time (Axelrod 1979) resulted in the invasion of more mesic environments of / / higher elevation by Oreortyx. The southward displacement of land west of the San Andreas Fault at this time might also have isolated this taxon (see Wenner and Johnson1980). Another east-westsplit of an ancestraltaxon resulted in the divergence of Colinus(Fig. 5b), estimated by our data at 7.0 MYBP. The earliest known fossils of Colinus(Holman 1961, Brodkorb 1964) are from the upper Plioceneof Kansas.Because our estimated divergencedate is well before upper Pliocene, the sites of fossil Colinusdo not permit identificationof the area of origin of Colinus. Penultimately, Callipeplaand Lophortyxdi- verged (Fig. 5c), about 2.8 MYBP, or late Plio- cene, when their ancestorwas fragmented in the southwestern aridlands of North America. Axelrod (1979)noted that during the late Plio- ceneisolated arid and semi-ariddesert patches existed in the current Sonoran and Chihua- huan desert regions, and this could have al- lowed the allopatricdifferentiation of Callipe- pla, which presently occupiessuch habitats (Leopoldet al. 1981).Species of Lophortyxdi- C...2.8M YB P I / C.v•;wbnus • verged last, resulting in the current distribu- tion patterns(Fig. 4). It will be of value to as- certainthe phylogeneticposition of L. douglasii. Hubbard (1973)proposed a vicariant biogeo- graphicexplanation for the evolutionof species in the generaLophortyx and Callipepla(consid-

consistingof evergreenchaparral, evergreen-broad- leaf forest, or coniferous forest with shrub under- story in western North America. B. Origin of Colinus virginianus,7.0 MYBP. Presenthabitat is essentially Fig. 5. Diagrammatic representation of hypo- weedy fields bordered by brush or woodlots, al- thetical stagesin the evolution of speciesshown in though in tropical lowlandsit occursin wetter con- Fig. 4. Becausehistorical ranges are unknown,ranges ditions. The exactlocation of the origin of C. virgin- should not be interpreted strictly. The primary in- ianus is uncertain. Note that the range of "pre" formationwe wish to conveyis the isolationevents, Callipepla-Lophortyxcould have extendedfurther east which are indicated by the dashedlines. The exact if C. virginianuswas either isolatedto the south or position of the dashedlines is speculative,however. north. C. Divergence of Callipeplasquamata and Lo- Therefore,whether differentiationamong these taxa phortyx, 2.8 MYBP, probably concurrent with late was parapatric or allopatric and the extent of any Pliocene disjunct patchesof arid and semi-arid des- gaps between taxa during their evolution are un- ert. C. squamataand L. gambeliiare typically found known. After each isolation event, dispersalproba- in desert scrub or arid grasslands,while L. califor- bly occurredacross these boundaries. A. Separation nicusoccurs in oak woodland, chaparral,and brushy of Oreortyxpictus, 12.6 MYBP, presumablyin areas foothills. 42 GUTIgRREZ,ZINK, ANDYANG [Auk, Vol. 100 ered by him congeneric),which involved hy- ed that L. garnbeliiand L. californicusare con- potheticalancestors and their distributionsand specific.The genetic data presentedhere are Pleistocene glaciation cycles. According to consistentwith this idea. Wild hybrids (Hen- Hubbard's scenario, a trichotomoussplit pro- shaw 1885, Miller and Stebbins 1964) between duced C. squarnata,L. douglasii,and "pre-cali- the formsinclude only the F1 generation,how- fornicus-garnbelii"in the Illinoian glacialepoch, ever, which suggestsa lack of introgressionand with L. californicusand L. garnbeliidifferen- panmixia in zones of sympatry. Furthermore, tiating in the Wisconsinianglacial period. Us- hybrids have been reported for other sym- ing the geneticdistance conversion established patrix quail [e.g. Colinusvirginianus x L. cali- above, we estimate the split of L. garnbeliiand fornicus(Aiken 1930);Callipepla squamata x L. L. californicusat 190,000 yr ago, and that of gambelii(Bailey 1928); L. californicusx C. squa- Lophortyx and Callipepla at 2.8 MYBP, or rnata (Jewett et al. 1953); C. virginianusx C. roughly late Pliocene. While Hubbard is cor- squarnata(Johnsgard 1973); O. pictus x L. cal- rect in assumingthat a minimum of two geo- ifornicus(Peck 1911)].Incidence of hybridiza- logic events (e.g. glacial-interglacialcycles) is tion is probably not an accuratepredictor of needed to accountfor the distribution patterns closephylogenetic relationship, becausebirds of extant Callipeplaand Lophortyx,these gen- retain the ability to hybridize despite consid- era probably divergedwell before the times he erable genetic divergence (Prager and Wilson suggested.Illinoian age glacialcycles may well 1975). The apparent lack of prereproductive have effected speciation in Lophortyx,how- isolatingbarriers in sympatry,at leastto F1hy- ever. bridization, does not necessarilyindicate re- This biogeographicreconstruction is a hy- cency of common ancestryor close phyloge- pothesis. We note that sympatry of breeding netic relationships among these quail. species, which is considerable among the Therefore, we reject the notion that hybrids speciesstudied here (Fig. 4), implies dispersal between L. garnbeliiand L. californicusprove (Nelson and Platnick 1981). Thus, it is difficult conspecificstatus. As only the F1 hybrids and to determine the relative importance of vicar- not a hybrid swarmhave been found, theseare iance or dispersalin accountingfor the evo- probably distinct biological species.We also lutionary patterns in this group. Also, geolog- point out that the evidence supporting appar- ical and paleobotanicalevidence is sufficiently ent assortativemating in sympatry overshad- fragmentary (see Axelrod 1979, Wenner and ows our finding a D-value typical of subspe- Johnson 1980) to prevent precise correlations ciesbetween these taxa. Clearlydistinct species with our phylogenetichypothesis. That is, we can be genicallysimilar (Avise et al. 1980b,c). lack a well corroborated "area cladogram" Several authors (e.g. Mayr and Short 1970, (Nelson and Platnick 1981). Johnsgard1973, and referencestherein) have Our phylogenetichypothesis and dating of suggestedmerging Lophortyxand Callipepla. cladogeneticevents suggest that a seriesof three Thesegenera are clearly similar (Fig. 1). The• east-west range disjunctions(Fig. 5) could ex- between our samplesof these two taxa, 0.104, plain the evolution of these genera of New is one-halfthat reportedby Barrowclough(1980) World quail. These patterns need to be corrob- for similar avian intergenericcomparisons; yet orated with studies of other avian groups, as it is within the range (0.0126-1.214).Thus, our well as other groups of vertebrates and non- data provide no clear-cutanswers, and we sug- vertebrates.We believe, however, that our hy- gestthat the decisionregarding their taxonom- pothesis(Fig. 5) is an important first approxi- ic status be made on the basis of other kinds mation of the evolutionaryhistory of thesequail of biological evidence. taxa and makes objective, testable predictions The suggestionby Phillips et al. (1964) and that would otherwise be difficult given only Mayr and Short (1970)that Oreortyxbe merged the map of currentbreeding distributions.We with Callipepla (including Lophortyx) is not also wish to demonstrate that molecular meth- consistentwith our moleculardata (Figs. 1-3). ods of inferring phylogeniescan be combined It would alsorequire inclusionof Colinus;oth- with information from the fossil record to fur- erwise, the new taxonwould not be monophy- ther understandingof evolutionarypatterns in letic. We think that merging these taxa would avian groups. obscure their relatively long, independent, Taxonorny.--Mayrand Short (1970) suggest- evolutionary histories. We recognize, how- January1983] GenicVariation in Galliforms 43 ever, that there can be no absolute value of AMERICAN ORNITHOLOGISTS' UNION. 1957. Check- genetic distanceon which to base taxonomic list of North American Birds, fifth ed. Baltimore, decisions. The external phenotypic resem- Maryland, Amer. Omithol. Union. blance of Mountain and California quail does 1973. Thirty-second supplementto the American Ornithologists' Union check-list of not, in this case, indicate a closephylogenetic North American birds. Auk 90: 411-419. relationship. Furthermore, Hudson et al. (1959, AvisE, J. C., J. C. PATTON,& C. F. AQUADRO. 1980a. 1966) and Holman (1961) provide data on the Evolutionarygenetics of birds. I. Relationships myology and skeletal morphology, respective- amongNorth Americanthrushes and allies.Auk ly, that show that Oreortyxis morphologically 97: 135-147. distinct from other membersof the Dendrortyx , --, & --. 1980b. Evolutionary ge- group. Gutierrez (1980)reported that Oreortyx netics of birds. II. Conservativeprotein evolu- was very differentecologically from Lophortyx. tion in North American sparrowsand relatives. Thus, genetic, morphologic,and ecologicdata Syst. Zool. 29: 323-334. show that Oreortyx is not a close relative of , --, & --.. 1980c. Evolutionary ge- netics of birds. Comparative molecularevolu- Lophortyxor Callipepla,and there seemsto be tion in New World warblers and rodents. J. He- no basis for their generic merger. redity 71: 303-310. The systematicstatus of C. virginianusis un- AXELROr),D. I. 1979. Age and origin of Sonoran certain. It is shown here to be a distinct clade desertvegetation. Occ. Papers,Cal. Acad. Sci. within the Odontophorinae and more similar to Lophortyxand Callipeplathan to Oreortyx AYALA, F.J. 1975. Genetic differentiation during and Cyrtonyx. the speciationprocess. Evol. Biol. 8: 1-78. Some authors(Brodkorb 1964, Mayr and Short BAILEY,V. 1928. A hybrid Scaledx Gambel'squail 1970,Johnsgard 1973) consider the Tetraonidae from New Mexico. Auk 45: 210. a subfamily of the Phasianidae. Our data (Ta- BARROWCLOUGH,G. F. 1980. Genetic and pheno- ble 1) show that the distance from T. pallidi- typic differentiation in a wood warbler (Genus Dendroica)hybrid zone. Auk 97: 655-668. cinctus(Tetraonidae) and P. colchicus(Phasian- --, & K. W. CORBIN. 1978. Genetic variation idae) to all other species is similar. Thus, it and differentiation in the Parulidae. Auk 95: 691- might be appropriateto considersuch a taxo- 702. nomic scheme. --, & R. M. ZINR. 1981. Genetic dif- ACKNOWLEDGMENTS ferentiationin the Procellariiformes.Comp. Bio- chem. Physiol. 69B: 629-632. We thank the following individuals for assisting BRODKORB,P. 1964. Catalog of fossil birds: part 2 in various ways with this project:John Davis, Rich- (Anseriformesthrough Galliformes). Bull. Flor- ard D. Sage,Vincent Sarich, Don Straney,Allan C. ida State Mus. Biol. Sci. 8: 195-335. Wilson, and J. W. Wilson. David E. Brown, Richard CORBIN,K. W. 1981. Genic heterozygosityin the Brown, Larry Caudill, Michael Erwin, Jim Gerber, White-crownedSparrow: a potential index to Dale Jones, A1 Woodard, and Tom Zapatka either boundaries between subspecies.Auk 98: 669- helped collectspecimens or provided useful locality 680. information. Ramone Baccus, George F. Barrow- F^RmS,J. S. 1972. Estimating phylogenetic trees clough,John E. Cadle, Kendall W. Corbin, Ned K. from distance matrices. Amer. Natur. 106: 645- Johnson,Allan Larson, A. Starker Leopold, Jill A. 668. Marten, Gareth Nelson, James L. Patton, Duke S. FELSENSTEIN,J. 1978. Cases in which parsimony Rogers,Charles G. Sibley, and David W. Steadman or compatibilitymethods will be positivelymis- providedhelpful comments on variousdrafts of this leading. Syst. Zool. 27: 401-410. paper. Julie Federassisted in the lab, and JeanneA. FITCH, W. g., & E. MARGOLIASH. 1967. Construc- Dawson typed the paper. Gene Christmandrew the tion of phylogenetictrees. Science 155: 279-284. figures.Dr. Donald E. Savageprovided dateson fos- GUTIf•RREZ,R. J. 1980. Comparativeecology of the sil localities. A Ford Foundation Fellowship to the Mountain and California quail in the Carmel first author, the Museum of VertebrateZoology, and Valley, California. Living Bird 18: 71-93. the Union Foundation Wildlife Fund furnished fi- HENNIG,W. 1966. Phylogeneticsystematics. Chi- nancialsupport. RMZ was supportedby NSF grant cago, Illinois, Univ. Illinois Press. DEB-7920694 to N. K. Johnson. HENSHAW,H. W. 1885. Hybrid quail (Lophortyx gambeliix L. californicus).Auk 2: 247-249. LITERATURE CITED HOLMAN,J. A. 1961. Osteologyof living and fossil AIREN, C. E. H. 1930. A Bobwhite x California New World quails (Aves, Galliformes).Bull. Florida State Mus. Biol. Sci. 6: 131-233. Quail hybrid. Auk 47: 80-81. 44 GUTff•RREZ,ZINK, ANDYANG [Auk, Vol. 100

1964. Osteology of gallinaceous birds. The birds of Arizona. Tucson, Arizona, Univ. Quart. J. Florida Acad. Sci. 27: 230-252. Arizona Press. HUBBARD,J. P. 1973. Avian evolution in the arid PRAGER, E. M., & A. C. WILSON. 1975. Slow evo- lands of North America. Living Bird 12: 155-196. lutionary loss of the potential for interspecific HUDSONßG. E., P. J. LANZILLOTTI,& G. D. EDWARD. hybridization in birds: a manifestation of slow 1959. Muscles of the pelvic limb in galliform regulatory evolution. Proc. Natl. Acad. Sci. 72: birds. Amer. Midl. Natur. 61: 1•37. 200-204. ßR. A. PARKER,J. VANDENBERGE, & P. J. LAN- ß& . 1976. Congruencyof phylogenies ZrLLOTTI. 1966. A numerical analysis of the derived from different proteins. J. Molec. Evol. modifications of the appendicular muscles in 9: 45-57. variousgenera of gallinaceousbirds. Amer. Midi. , A. H. BRUSH, R. A. NOLAN, M. NAKANISHI, Natur. 76: 1-73. & A. C. WrLSON. 1974. Slow evolution of JEWETT,S. G., W. P. TAYLOR, W. T. SHAW, & J. W. transferrin and albumin in birds accordingto ALDRICH. 1953. Birds of WashingtonState. Se- micro-complement fixation analysis. J. Molec. attle, Washington, Univ. Washington Press. Evol. 3: 243-262. JOHNSGARD,P.A. 1973. Grouseand quails of North PRESCH,W. 1979. Pheneticanalysis of a single data America. Lincoln, Nebraskaß Univ. Nebraska set: phylogenetic implications. Syst. Zool. 28: Press. 366-371. JOHNSONßM. S., & J. L. BROWN. 1980. Genetic vari- ROGERS,J. S. 1972. Measuresof geneticsimilarity ation among trait groups and apparent absence and genetic distance. Studies in Genetics VII. of close inbreeding in Grey-crowned Babblers. Univ. Texas Publ. 7213: 145-153. Behav. Ecol. Sociobiol. 7: 93-98. SARICH,V. M. 1977. Rates, sample sizes, and the JOLL•S, J., I. M. IBRAHIMI, E. M. PRAGER, F. neutrality hypothesisfor electrophoresisin evo- SCHOENTGEN,P. JOLLES,& A. C. WILSON. 1979. lutionary studies. Nature 265: 24-28. Amino acid sequence of pheasant lysozyme. SELANDER, R. K., M. H. SMITH, S. Y. YANG, W. E. Evolutionarychange affecting processing of pre- JOHNSON, & J. B. GENTRY. 1971. Biochemical lysozyme. Blochem. 13: 2744-2752. polymorphism and systematicsin the genus LEOPOLD,A. S., R. J. GUTIERREZ,& M. T. BRONSON. Peromyscus.I. Variation in the old-field mouse 1981. North American game birds and mam- (Peromyscuspolionotus). Studies in GeneticsVI. mals. New York, Charles Scribner's Sons. Univ. Texas Publ. 7103: 49-90. MAXSON,L. R., & R. D. MAXSON. 1979. Compar- SIBLEY, C. G., & J. E. AHLQUIST. 1982. The rela- ative albumin and biochemical evolution in tionships of the Yellow-breasted Chat (Icteria vi- plethodontid salamanders. Evolution 33: 1057- rens) and the alleged slowdown in rate of mac- 1062. romolecular evolution in birds. Postilia 187: 1- MAYR, E., & L. L. SHORT. 1970. Speciestaxa of 18. North American birds. Publ. Nuttall Ornithol. SNEATH, P. H. A., & R. R. SOKAL. 1973. Numerical Club 9: 1-127. taxonomy. San Francisco,W. H. Freeman & Co. MrLLER, A. H., & R. C. STEBBINS. 1964. The lives TEMPLETON,A. R. 1980. Modes of speciation and of desert animals in Joshua Tree National Mon- inferencesbased on geneticdistances. Evolution ument. Berkeley,California, Univ. Calif. Press. 34: 719-729. NEI, M. 1975. Molecular population genetics and WAKE,D.B. 1981. The applicationof allozymeevi- evolution. Amsterdam, North Holland. dence to problems in the evolution of morphol- 1978. Estimationof averageheterozygosity ogy. Pp. 257-270 in Evolution today (G. G. E. and geneticdistance from a smallnumber of in- Scudder and J. L. Reveal, Eds.). Proc. 2nd Inter- dividuals. Genetics 89: 583-590. natl. Congr. Syst. Evol. Biol. NELSON,G., & N. G. PLATNICK. 1981. Systematics WENNER, A.M., & D. L. JOHNSON. 1980. Land ver- and biogeography.New York, Columbia Univ. tebrates on the California Channel Islands: Press. sweepstakesor bridges:Pp. 497-530in The Cal- NEro, E. 1978. Genetic variation in natural pop- ifornia Islands: proceedingsof a multidiscipli- ulations:patterns and theory. Theor. Pop. Biol. nary symposium(D. M. Power, Ed.). Santa Bar- 13: 121-177. bara, California, Santa Barbara Mus. Nat. Hist. PECK,M. E. 1911. A hybrid quail. Condor 13: 149- YANG, S. Y., & J. L. PATTON. 1981. Genic variabil- 151. ity and differentiationin the Galapagosfinches. PETERS,J. L. 1934. Check-list of birds of the world, Auk 98: 230-242. vol. 2. Cambridge,Massachusetts, Harvard Univ. ZINK, R. M. 1982. Patterns of genic and morpho- Press. logic variation among sparrowsin the genera PHrLLrPS,A. R., J. MARSHALL, & G. MONSON. 1964. Zonotrichia,Melospiza, lunco, and Passerella.Auk 99: 632649. January1983] GenicVariation in Galliforms 45

APPENDIX1. Location,sample sizes, and samplecollection dates. Different populationsof the sametaxon are labeledby upper caseletters, which correspondto the lettersused in Appendix2, Table 1, and the figures. The taxonomicframework is from Peters (1934).

Number of indi- Taxon viduals Locality and date

Tetraonidae Lesser Prairie Chicken 13 New Mexico: 8 mi E Milnesand, Roosevelt Co., Decem- (Tympanuchuspallidicinctus ) ber 1975. Phasianidae Phasianinae Ring-neckedPheasant 13 California: Webb Tract, Sacramento Delta, Sacramento (Phasianuscolchicus ) Co., November 1975. Perdicinae Common Quail 30 Avian SciencesDepartment, University of California, (Coturnix coturnix) Davis, California, A--Big Brown Strain (n = 10). B-- Small Brown Strain (n = 10). C--Albino Strain (n = 10). A, B, and C obtained in February 1976. Chukar 12 Avian Sci. Dept., Univ. Calif., Davis. (n = 10), Febru- (Alectorischukar) ary 1976;5 mi SE Panoche,San Benito Co., California (n = 2), Jan. 1976; samplescombined. Odontophorinae DendrortyxGroup California Quail 36 California: A--5 mi E Shahdon, San Luis Obispo Co. (Lophortyxcalifornicus ) (n = 6), December 1974. B•5 mi N Jolon, Monterey Co. (n = 13), December 1974. C•4 mi E Mercy Hot Springs,Fresno Co. (n = 9), October1975 and (n = 2) in January1976; 5 mi SE Panoche,San Benito Co. (n = 6), January1976. Gambel's Quail 22 New Mexico: 1 mi E Columbus, Luna Co. (n = 19), De- (L. gambelii) cember 1975. Arizona: 10 mi E Green Valley, Pima Co. (n = 3), January 1976; samplescombined. Scaled Quail 29 New Mexico: A•8 mi E Milnesand, Roosevelt Co. (n = (Callipeplasquamata ) 7), December 1975. B--1 mi E Columbus, Luna Co. (n = 20), December 1975. Arizona: 10 mi E Green Valley, Pima Co. (n = 2), January1976; combined with population B as there was no differentiation. Bobwhite Quail 15 New Mexico: A--8 mi E Milnesand, Roosevelt Co. (n = (Colinusvirginianus ) 8), December 1975. B--18 mi NE Milnesand, Roose- velt Co. (n = 7), December 1975. Mountain Quail 16 California: 2 mi SE Jamesburg,Monterey Co. (n = 16), (Oreortyxpictus) June-August 1975. OdontophorusGroup Montezuma Quail 31 Arizona: A--15 mi E Patagonia, Santa Cruz Co. (n = (Cyrtonyxrnontezumae ) 23), January1976; B--10 mi W Patagonia,Santa Cruz Co. (n = 8), January 1976. 46 GUTIERREZ,ZINK, ANDY^NG [Auk, Vol. 100

APPEND/X2. Allelic frequenciesfor 23 presumptiveloci in 10 speciesof gallinaceousbirds. Numbers in parenthesesare frequenciesof allelesat a locus. A singleletter denotessample fixed for that allele. Full names for loci given in Yang and Patton (1981) or below. Names of taxa and samplesizes given in Ta- ble 1.

Locus T.p. P.c. C.c. A C.c. B C.c. C A.c. L.g. L.c. A PGI b c d (0.65) d (0.60) e c b b e (0.35) e (0.40) ADA • g b d (0.35) f f e a (0.42) a (0.06) f (0.65) c (0.58) c (0.94) PGM-1 a c d d d d b b

MPI h c f e (0.60) f a e e (0.94) f (0.40) g (0.06)

IDH-1 e d c c c d a (0.97) a f (0.03) IDH-2 g b g g g a (0.30) f f c (0.70) c•GPD-1 d c e e e a b b c•GPD-2 c c d d d a b b

ME•' g d (0.12) a (0.25) a (0.45) a (0.40) f f e (0.03) e (0.88) b (0.75) b (0.55) b (0.60) f (0.97) GOT-1 i j h h h a (0.45) g (0.97) g b (0.05) i (0.03) c (0.50) GOT-2 a b b b b a b b GDH •' a c b b b b b b UDH ci d d d d d d c c SDH a e a a a b (0.15) d d c (0.85) LDH-1 a a c c c b b b LDH-2 a a c c c b b b Pept-1 g a b b b a c c

Pept-2 d d e e e a b b Alb g c d (0.95) c (0.40) c b e c (0.12) f (0.05) f (0.60) e (0.88) Est-1 a c (0.08) e d (0.60) e f f (0.05) f (0.03) d (0.92) e (0.40) g (0.95) g (0.97)

Est-2 g g (0.38) f f f e b a (0.03) h (0.62) b (0.97) 6PGD d g f (0.85) e (0.05) f (0.75) c (0.10) d b (0.03) h (0.15) f (0.80) h (0.25) d (0.90) d (0.97) h (0.15) XDH • g f a (0.30) b (0.05) a (0.20) c a (0.08) a (0.03) c (0.70) c (0.95) c (0.80) c (0.92) c (0.97) Percentage poly- morphism 0.0 11.1 22.2 25.9 11.1 14.8 18.5 29.6 Hetero- zygosity 0.0 2.6 4.8 8.9 4.8 5.2 2.5 2.8 Mean number alleles per poly- morphic locus 2.0 2.0 2.1 2.0 2.2 2.0 2.0

"Adenosene de-aminase. t'Malic enzyme(NADP dependent). • Glutamatedehydrogenase. d Unidentifieddehydrogenase. • Xanthine dehydrogenase. January1983] GenicVariation in Galliforms 47

APPENDIX 2. Continued

L.c. B L.c. C C.s. A C.s. B C.v. A C.v. B O.p. C.m. A C.m. B

b b b b b b a b b

c c a a (0.75) a (0.56) a (0.50) e (0.97) c c c (0.25) c (0.44) c (0.50) g (0.03) b b (0.96) c c c c b c c d (0.04) e (0.83) e (0.92) e e (0.75) d d b g (0.91) g (0.94) g (0.17) c (0.04) g (0.25) i (0.09) i (0.06) g (0.04) a a a a a a (0.93) a b b c (0.07) f c (0.11) f f f f f d (0.04) e (0.94) f (0.89) e (0.96) g (0.06) b b b b b b b b b b b b b b b b b (0.85) b (0.87) d (0.15) d (0.13) f f f f b (0.06) e c e e e (0.94) g g (0.92) g (0.71) f (0.05) d (0.06) g g g e (0.13) i (0.08) j (0.29) g (0.70) g (0.94) g (0.87) j (0.25) b b b b b b b b b b b b b b b b b b c c c c c c b a a d d d d d d b (0.63) b b d (0.37) b b b b b b b b b b b b b b b b b b c c c c (0.97) d d c (0.06) e e f (0.03) f (0.94) b b b b b b b c c c (0.08) c (0.15) e e a a e a a e (0.92) e (0.85) g g g g h h f a (0.83) a (0.87) b (0.15) b (0.13) c (0.02) b b b b b b s c b (0.19) c (0.81) d d d d d b (0.07) d d (0.96) d d (0.93) f (0.04)

c c a (0.07) a (0.10) a (0.94) a (0.86) f e e d (0.93) d (0.90) e (0.06) e (0.14)

7.4 18.5 7.4 18.5 14.8 14.8 11.1 18.5 22.2

1.8 3.4 1.6 3.7 2.8 2.6 2.1 2.4 5.1

2.0 2.2 2.0 2.2 2.0 2.0 2.0 2.2 2.0