The Condor89:377-386 0 The Cooper Ornithological Society 1987

EVIDENCE OF HYBRIDIZATION BETWEEN RED-BELLIED AND GOLDEN-FRONTED ’

JULIA I. SMITHY Department of Zoology, Universityof Oklahoma, Norman, OK 73019

Abstract. Golden-frontedWoodpeckers ( aurifrons) and Red-belliedWood- peckers(M. carolinus)are sympatricfrom southwesternOklahoma to easternTexas. Earlier studiesfound no evidenceof hybridization(Selander and Giller 1963). However,in the recentpast the area of range overlap betweenthese two specieshas increased,thereby increasingthe opportunityfor hybridization.I investigatedthe possibilityof hybridization by analyzingmorphological and electrophoreticcharacteristics. Twenty-five (15.8%) indi- vidualswith intermediatemorphologies were collected within the areaof overlapand were identified as putative hybrids. Electrophoreticanalysis of 12 liver and muscleproteins revealeda closegenie affinity between the two species.Individual geniecomplements within the zone of overlap indicate that some individuals are intermediate.The intermediate morphologyand mixed geniecomposition of someindividuals within the zone of overlap supportsthe conclusionthat Red-belliedand Golden-frontedwoodpeckers hybridize. Key words: Red-belliedWoodpecker; Melanerpes carolinus; Golden-fronted ; Melanerpesaurifrons; hybridization.

INTRODUCTION tending from southwestern Oklahoma to the The purpose of my study was to investigate the Texas Gulf Coast (Fig. 1); this zone corresponds, possibility of hybridization between the Red-bel- in part, to the Western Cross Timbers of central lied Woodpecker (Melanerpes carolinus) and the Texas (Dyksterhuis 1948). The Cross Timbers Golden-fronted Woodpecker (M. aurifvons). phytogeographicregion is characterized by the These two woodpeckers are members of a me- interdigitation of northeastern mesic oak wood- lanerpine superspeciescomposed of five mor- lands, with southwestern semi-arid Savannah phologically and behaviorally similar species: (Hamilton 1962). Thus, it is a biotically inter- Red-bellied Woodpecker, Golden-fronted mediate zone composed of Red-bellied and Woodpecker, Gila Woodpecker (M. uropygialis), Golden-fronted woodpecker habitat. Hoffmann’s Woodpecker (M. hoflmannii), and Hybridization- the crossingof individuals be- Great Red-bellied Woodpecker (&f. superciliaris; longing to two unlike populations that have sec- Short 1982). The Red-bellied Woodpecker is ondarily come into contact (Mayr 1970)-has found throughout the south-central and eastern been noted for several pairs of North American United States, where it inhabits mesic areas of forms that are classifiedas different species swampy woods, open deciduouswoodlands, and (Rising 1983). Many of these pairs meet and hy- mixed coniferous woodlands (Bent 1939). The bridize in ecologicallyintermediate areas such as Golden-fronted Woodpecker rangesfrom south- contact zones between two biotas (Remington western Oklahoma to Honduras. In Texas and 1968). In Mexico, hybridization occurswhere the Oklahoma, Golden-fronted Woodpeckers occu- range of the Golden-fronted Woodpecker over- py xeric habitats of mixed oak-juniper-mesquite laps with the Gila Woodpecker (Short 1982). woodlands as well as riparian woodlands of cot- Likewise, in Honduras the Golden-fronted tonwood, willow, and cypress(Selander and Gill- Woodpeckermeets Hoffmann’s Woodpecker and er 1963). At present, the Golden-fronted Wood- purported hybrids have been observed (Short pecker meets the Red-bellied Woodpecker in 1982). In central Texas, however, accounts of favorable habitats within a zone of overlap ex- hybridization between Golden-fronted and Red- bellied woodpeckershave not been substantiated (Selander and Giller 1963). I Received5 June 1986.Final acceptance2 January 1987. Selander and Giller (1963) reported that the 2 Presentaddress: Museum of VertebrateZoology, northern breeding limit of Golden-fronted Universityof ,Berkeley, Berkeley, CA 94720. Woodpeckers in Oklahoma was near Gould.

13771 318 JULIA I. SMITH

FIGURE 1. Geographic area of study, and rangesof Red-bellied and Golden-fronted woodpeckers.

However, Wood and Schnell(l984) depicted the northern limit of Golden-fronted Woodpecker permanent residency as extending beyond Gould well into southwestern Oklahoma. Similarly, in FIGURE 2. Projections of (a) female and (b) male 193 1 the southwestern limit of Red-bellied individuals from (c) eight localities onto an adjusted Woodpeckers was thought to be near Lawton, principal component I. For females, scores on com- Oklahoma (Sutton 1967). However, by 1970 they ponent I adjustedby subtracting0.603. Similarly, male component adjusted by subtracting 0.610 from all were found well into southwesternOklahoma to scores. Putative hybrids designated by arrows and the Texas border (Tyler 1979). Apparently, with- brackets. in the recent past, both the Golden-fronted and Red-bellied woodpecker have extended their range into southwestern Oklahoma, thereby in- and pattern of morphological variation. I ex- creasingthe area of their sympatry. My objective amined only adult in breeding condition was to determine whether these two woodpeck- to insure that: (1) individuals were residents in ers hybridize and, if so, to estimate the frequency the area collected, (2) plumages were not worn; of hybridization. The analyses concentrated on and (3) age differencesin plumage pattern would assessing morphometric and electrophoretic not confound the results. Specimen collection characteristicsof Golden-fronted and Red-bel- sites were grouped into eight physiographically lied woodpeckers in the zone of potential hy- homogeneouslocalities (Fig. 2~). bridization, as well as beyond the overlap region. Twenty-one characters were assessedfor fe- males and 25 for males. I measured the following METHODS eight morphometric charactersto the nearest 0.1 MORPHOLOGICAL ANALYSIS mm with dial calipers: (1) tail length on longest Study skins of female (n = 96) and male (n = central rectrix from base to tip; (2) bill length 176) Red-bellied and Golden-fronted wood- from anterior edge of nostril to tip of bill; (3) bill peckers from Oklahoma, Texas, and southern depth from top of culmen to base of lower man- Kansas were analyzed to determine the degree dible at anterior edge of nostril; (4) length of WOODPECKER HYBRIDIZATION 379 tarsus from tip of heel scale to base of third toe; plete gray gap between nape and cap (2). Color (5) wing length of the flattened arc; (6) height of of chin: red (0) to yellow (3). Subdominant color black tail bar at midpoint of tail length (if black of nape: color of lateral side of nape not different bars not present, character scored as “no com- from central portion (0), to lateral side orange parison”; Sneath and Sokal 1973); (7) height of (3). white tail bar at middle of central rectrix (ifwhite Specimens with five or more missing values bars not present, character scored as no com- were excluded from all analyses. The missing parison); and (8) length of left third toe along values of the remaining damaged specimenswere lateral border from base of toe pad to tip of pad. estimated by a linear regression onto the char- I analyzed plumage variation by assessingthe acter that exhibited the highest correlation with color of the front, nape, belly, and cap (males the missing character (Missing Data Estimator only). Colors were measured by illuminating a program developed by D. M. Power; Schnell et specimen with a Standard Macbeth Artificial al. 1985b). The estimateddata accountedfor only North Sky Daylight lamp and matching the color 3.4% (69 of 2,016) of female and 2.5% (111 of of the plumage to a referencecolor chip from the 4,440) of male measurements. Munsell Limit Color Cascade (Munsell Color Sexual dimorphism occursin both species(Se- 1970). Different refractory angles can alter the lander 1966, Wallace 1974) so all analyses were structural colorsof plumages;thus, I viewed each performed separately by sex. Data matrices for plumage region from a consistent angle while both sexeswere standardized, characterscorre- holding the specimen under the light source. lated, and principal components extracted.When For each plumage region, Munsell Hue, Value, more than 15% of the values for one character and Chroma were recorded. Munsell Hue indi- were estimated, I examined whether these esti- cates the position of a particular color relative mated values altered the projection of individ- to an equally spaced scale of hues from red to uals onto the first principal component. In each purple. The plumage colors I assessedranged case, this treatment of missing values did not from red to yellow. In the Munsell Limit Color appreciably influence projections. Numerical CascadeSystem of notation, red hues are ranked procedureswere performed using NT-SYS com- zero to 10, oranges are represented by values puter programs (Rohlf et al. 1982). from 10 to 20, and yellows range from 20 to 30. Following the suggestion of Moore and Bu- In a general sense,Munsell Hue correspondsto chanan (1985) I summarized variation between the dominant wavelength of a color. Munsell Red-bellied and Golden-fronted woodpeckers Value indicates lightness and is related to the with principal component I. To center near zero percent spectral reflectance of color. It ranges the projections of individuals with intermediate from zero for absolute black to 10 for absolute morphologies, a constant was subtracted from white. Munsell Chroma describesthe degree of all principal component I scores. saturation of a color and represents excitation There are two underlying assumptions to this purity. A neutral gray would have a Munsell method of hybrid identification. First, principal Chroma of zero. For a detailed description of the component I must describe the variation rele- relationship of Munsell notations to dominant vant to the question of hybridization. Neff and wavelength, percent spectralreflectance, and ex- Smith (1979) indicated that principal component citation purity, the reader is referred to Newhall analysis is a good way to analyze hybridization et al. (1943). and eliminates many of the erroneous compu- I evaluated variation in five plumage patterns tational assumptions of other methods (e.g., dis- by ranking observed forms from lowest (Red- criminant function analysis). By definition, the bellied Woodpecker type) to highest (Golden- first component is the axis that summarizes the fronted Woodpecker type) for the following char- greatestamount of variation among the elements acters. Tail pattern: white bars on central rec- of a data matrix. Thus, it may best represent the trices extend from central rachis to outer edge of differencesbetween the parental speciesand pro- vane (0) to no white on central rectrices(3). Back vide an adequate means of identifying hybrids. pattern: black bars on the back wider than white Specifically, hybrids would be those individuals (0), white bars on back equal to or wider than lying between species’ clusters and yet outside black bars (1). Nape gap coloration (males only): the limits of either species’ variation. no gray gap between nape and cap (0), to com- The second assumption-that hybrids exhibit 380 JULIA I. SMITH phenotypes intermediate to the two parental 197 1) and followed the staining procedures of forms (Neff and Smith 1979)-will hold if there Harris and Hopkinson (1976). I studied six loci is additive inheritance of traits or a combination from muscle tissue: aconitase (ACON-l), sor- of additivity and dominance (Rohwer 1972). For bitol dehydrogenase (SDH), alpha glucophos- fish, hybrids are not necessarily intermediate in phate dehydrogenase (AGPD), phosphogluco- all characters analyzed (Smith 1973, Ross and mutase (PGM), and leucyl-tyrosine (LT-1 and Cavender 198 l), but often are intermediate for LT-2). I also analysed six loci from liver tissue: many characters(Neff and Smith 1979, Mayhew lactate dehydrogenase (LDH- 1 and LDH-2) 1983). Principal component analysis is sensitive malate dehydrogenase (MDH- 1 and MDH-2), to the covariation of many charactersand rela- glycerol dehydrogenase (GCDH), aconitase tively insensitive to unique extremes (Smith (ACON-2), naphthyl acetase (NAS), and beta 1973). If a majority of the characters loading naphthyl phosphotase(BNP). The LDH, MDH, heavily on the first principal component are and GCDH loci were applied only in an exam- products of additive inheritance and a minority ination ofpossible species-specificfixed allele dif- are subject to control via other genetic mecha- ferences. Precise conditions of gel and buffer nisms, the first principal component can be ex- compositions can be obtained from the author. pected to depict phenotypes of hybrids as inter- Mobility of alleles at a locus was judged in ref- mediate. Since genetic mechanisms governing erenceto the position of the most common allele inheritance of the characters I assessedare un- designated “C,” with slower alleles (closer to the known, hybrid phenotypes cannot be indisput- origin) designated“ D.” Allele frequenciesfor each ably identified as intermediate. Thus, individu- locality were computed using the BIOSYS-1 als with intermediate phenotypes are designated computer program (Swoffordand Selander 198 1). as putative hybrids. I employed a Mantel test of matrix correlation (a procedure that compares the association of ELECTROPHORETIC ANALYSIS elements in two square difference matrices; Red-bellied and Golden-fronted woodpeckers Schnellet al. 1985a) to examine geographictrends (n = 93) were collectedfrom 20 counties in Okla- in allele frequency for polymorphic loci. Because homa and Texas: Oklahoma-Cleveland (n = 9) the number of localities (n = 18) compared was Caddo (1) Woodward (3), Ellis (8) Beckham (7), near the lower limit of reliability for the Mantel Greer (5), Harmon (9) Jackson(l), Marshall (3), statistic, I confirmed the result of each Mantel Love (3) and Johnston(3); Texas-Hemphill (n = test with a two-tailed permutational Mantel test 3), Cottle (S), Fannin (2) Williamson (4), Burle- (Schnell et al. 1985a) that employs a Monte Carlo son (2), Kimble (9), Kerr (1) LaSalle (6) and simulation. The critical value of the Mantel sta- McMullen (6). Specimens from Hemphill Coun- tistic (t) is 1.96 for a positive association and ty were collected in November; all others were - 1.96 for a significant negative association. The obtained from March to August. Monte Carlo probability (P) indicates significant Individuals from Kerr and Burleson counties covariation if P is greater than 0.975 or lessthan could not be scoredfor all loci studied. Nei (1978) 0.025. argued that estimates of genie variability are en- To determine whether there are regional geo- hanced more by increasesin the number of loci graphic patterns in allele frequency differences assessedthan by increasesin the number of in- for polymorphic loci, I compared the covariation dividuals sampled. Consequently, rather than between a matrix of allele frequency differences excluding loci that had not been scored for all among all localities to a corresponding matrix of individuals, I maximized the number of loci in- Euclidean distances (kilometers) among locali- vestigated by adding individuals not scored for ties. To test for local patterning of allele fre- all loci to the samples of nearby localities. quency, I compared allele frequency differences In the field, I removed pectoral muscle and among localities to a matrix of reciprocal geo- liver tissuefrom each individual and storedthem graphic distances. Employing reciprocals of dis- in liquid nitrogen or on dry ice until they could tance results in an expansion of short distances be transferred to a freezer and maintained at and increasesthe sensitivity of the test to asso- -70°C. At the Savannah River Ecology Labo- ciations among small distances (Schnell et al. ratory, I analyzed samples using standard starch 1985a). Using the Mantel test, I also assessedthe gel electrophoretic techniques (Selander et al. degree of covariation between genetic distances WOODPECKER HYBRIDIZATION 381

TABLE 1. Charactermeans, standard deviations (SD), and loadingson principalcomponent I for femalesand males.Eigen values for femalesand maleswere 10.4 and 9.9, respectively.

Female Male Character Meall SD Loading MeaIl SD Loading Tail length 79.1 4.77 0.277 81.5 5.25 0.370 Bill length 23.3 1.51 0.613 25.3 1.50 0.619 Bill depth 7.2 0.38 0.185 7.8 0.47 0.089 Tarsus 18.5 1.33 0.638 19.1 1.12 0.554 Wing length 125.7 4.78 0.343 129.3 4.12 0.384 Blacktail bar 4.1 1.08 -0.927 3.6 0.86 -0.844 White tail bar 4.2 0.71 -0.916 4.3 0.68 -0.847 Toe length 15.0 0.94 0.607 15.5 0.78 0.541 Front hue 16.1 5.89 0.947 15.6 5.64 0.958 Front value 7.2 0.94 0.916 6.8 1.19 0.946 Front chroma 13.3 2.05 -0.253 15.1 1.81 -0.547 Nape hue 14.5 5.51 0.942 10.4 2.55 0.691 Nape value 6.3 1.41 0.955 5.3 0.97 0.776 Nape chroma 15.7 1.13 -0.529 16.3 0.58 0.329 Belly hue 16.3 5.87 0.961 16.0 6.17 0.952 Belly value 7.2 0.95 0.913 7.0 1.16 0.915 Belly chroma 13.4 2.57 -0.210 14.4 1.88 -0.315 Cap hue _a - - 7.7 0.83 -0.082 Cap value - - - 3.9 0.36 0.029 Cap chroma - - 15.0 1.40 -0.015 Tail pattern 1.3 1.25 0.939 1.5 1.29 0.941 Back pattern 0.4 0.49 0.372 0.4 0.49 0.333 Nape gap color - - 0.7 0.76 0.840 Chin color 1.2 0.59 -0.311 1.4 0.86 0.014 Lateral nape color 0.2 0.60 0.164 1.1 1.09 0.827

aMeasurement not taken

and average taxonomic distances of individuals from the influence of possible hybrids and back- (n = 56) assessedfor both electrophoretic and crosses(Johnson and Johnson 1985). I repre- morphological variation. Nei’s (1978) unbiased sented typical morphological variation in Red- genetic distances were estimated among indi- bellied Woodpeckers as the level depicted by the viduals using the BIOSYS- 1 computer program range of principal component I scoresin the lo- (Swofford and Selander 198 l), and average taxo- cality farthest northeast of the overlap zone (lo- nomic distanceswere computed by the NT-SYS cality 1; Fig. 2~). In this locality the morphology computer program (Rohlf et al. 1982). The SDH of female and male Red-bellied Woodpeckers is locus was omitted from this test because it was describedby scoresnear the lower range of com- not scored for all individuals. ponent I (Figs. 2a, b). Similarly, becauselocality 8 (Fig. 2c) is farthest south of the contact zone, RESULTS I used component I scoresof females and males from that region to representmorphological vari- MORPHOLOGICAL VARIATION ation in Golden-fronted Woodpeckers (Figs. 2a, The charactersloading most heavily (greaterthan b). Golden-fronted Woodpeckers have pheno- 0.700) on principal component I for both females types that project as high values on component and males were: tail pattern; widths of tail bars; I (Fig. 2). coloration of front, nape, and belly (Table 1). Female Red-bellied and Golden-fronted Component I summarized 47.2% of the variance woodpeckers are morphologically more readily for females and 41.1% for males. Descriptive separablethan are males. There is a wide gap in statistics and character loadings on component female component I scoresbetween localities 1 I are summarized in Table 1. and 8, and only a small gap between the scores To measure the extent of hybridization, pa- of the males (Fig. 2). I identified female putative rental populations typically are sampled away hybrids (n = 4; Fig. 2) as those individuals of 382 JULIA I. SMITH

Oklahoma. In addition, there is less of a dis- tinction in the nape hue characterbetween males of the two speciesthan females. Throughout the eight localities, male nape hue ranges from red (8.5) to orange (14.3), whereasfor females, north to south, the color of the nape ranges from red (9.1) to yellow (20.2). I identified as putative hybrids 16 intermedi- ate males that were collected from localities 2, 3, 4, and 6. These males represent 15.2% of the males (n = 105) analyzed from the overlap region (i.e., localities 2, 3, 4, 5, and 6). To define more precisely the gap of component I scoresbetween males of the two species,I incorporated an ad- ditional intralocality measure of morphological variation. For each locality, the putative hybrid range was defined as the set of intermediate com- ponent I scoresclearly separate from scores of males with typical parental morphology. Em- ploying this method, I identified five additional putative male hybrids. In all, 21 putative male hybrids were found within and near to the zone of overlap (seeFig. 2b). Thus male hybrids com- prise approximately 17% of the population with- in the overlap zone. The estimated proportion of male hybrids rangesfrom a conservative 15.2% (n = 16) to as great as 20.0% (n = 2 1). In general, putative male hybrids resemble their female FIGURE 3. Allele frequenciesat six polymorphic loci counterpartsbeing characterizedby: no tail bars, representedfor 18 localities. only white blotches; reddish-orange to orange fronts; orangeto yellowish-orangebellies; no gray intermediate morphology lying within this wide gap on nape; and no extra lateral color on nape. gap of component I scores.These four specimens were collected from localities that are contained in part or completely within the zone of overlap GENETIC VARIATION (Figs. 2a, c). The hybrids represent 7.5% of the My electrophoretic analysis of genetic variation females (n = 53) analyzed from the area of range revealed that Red-bellied Woodpeckers and overlap (i.e., localities 2, 3, 4, 5, and 6). Female Golden-fronted Woodpeckers have a close ge- hybrid morphology is characterized by: large netic affinity. From a survey of 12 loci, I found white blotches on their tails, no true tail bars; no fixed allele differencesbetween the two species. orangeto yellowish-orange fronts; red napes;and Seven loci were polymorphic: AGPD, BNP, NAS, orange to yellowish-orange bellies. SDH, ACON-2, PGM, and LT-1. The AGPD Males of the two speciesexhibit a considerable locus, while polymorphic, was only variable at degreeof morphological variation. For example, two localities and, therefore, was not considered there are two Red-bellied Woodpecker speci- in the discussionofgeographic patterns ofgenetic mens from locality 1 with scoresnear zero. Be- variation. cause they were collected from areas consider- Two of the six polymorphic loci-PGM and ably beyond the suspectedzone of overlap, it is ACON- -demonstrated strong positive asso- unlikely that their intermediate phenotypes are ciations of allele frequency differenceswith geo- a result of hybridization (Rohwer and Kilgore graphic distances (i.e., regional patterning), in- 1973). In particular, the individual from locality dicating that for both loci the B and C allele 1 with the highestscore was collected in southern frequencies of geographically close localities are Kansas while the other was from east-central more similar than those for distant localities (Ta- WOODPECKER HYBRIDIZATION 383

TABLE 2. Associationofallele frequencydifferences with geographicdistances (km) and reciprocalsof distances (l/km), with Mantel statistic (t), Monte Carlo probability (P), and matrix correlation (r).

Locusand Distance(km) Reciprocaldistance (l/km) alleles f P i- f P i- ACON- B 4.083 0.997 0.486 -3.919 0.002 -0.403 C 4.659 0.999 0.522 -4.421 0.00 1 -0.435 PGM B 3.682 0.997 0.586 -3.654 0.000 -0.468 C 3.559 0.995 0.559 -3.504 0.000 -0.444 SDH C -0.469 0.549 -0.007 -0.679 0.214 -0.085 D -0.469 0.563 -0.007 -0.679 0.224 -0.085 NAS C -0.619 0.288 -0.080 0.909 0.815 0.099 D -0.619 0.320 -0.080 0.090 0.806 0.099 LT- 1 B -1.030 0.122 -0.111 0.768 0.744 0.074 C -1.260 0.064 -0.104 0.827 0.776 0.068 BNP : 0.1110.284 0.5610.651 0.0380.00 1 -0.7830.395 0.6330.241 -0.0870.041

D 1.239 0.863 0.144 -1.501 0.08 1 -0.152 E 1.080 0.866 0.108 -1.717 0.064 -0.158

ble 2, Fig. 3). For the B and C alleles of both southwestern Oklahoma and nearby north-cen- ACON- and PGM loci, allele frequency differ- tral Texas (Harmon and Cottle counties, respec- ences are negatively associatedwith reciprocals tively), populations are composedof individuals of geographicdistances (i.e., local patterning; Ta- with Golden-fronted Woodpecker morphology. ble 2 and Fig. 3). The significant regional and However, the genie constitutions of individuals local patterning of B and C allele frequencies (at in thesecounties include alleles common for both both the PGM and ACON- loci) reflects the Red-bellied and Golden-fronted woodpeckers fact that these alleles can be identified as most (Table 3). For example, most individuals have common for one of the two species.For example, the PGM allele most common for Red-bellied the B allele of PGM and of ACON- is most Woodpeckers (C), but the ACON- allele most common in Golden-fronted Woodpecker pop- common for the Golden-fronted Woodpeckers ulations of southern Texas (Fig. 3). In contrast, (B; Table 3). Similarly, mixed genie composi- the C allele at these two loci is most common in tions are found near the zone of overlap in east- northern samples of Red-bellied Woodpeckers central Texas (Williamson County); individuals (Fig. 3). The four other polymorphic loci tested exhibited Red-bellied Woodpecker plumages,yet did not show significant local or regional patterns at the ACON- locus many of them possessed (Table 2). the B allele that is most common in Golden- To investigate the significant local patterning fronted Woodpeckers. of the PGM and ACON- loci more fully, I ex- The Mantel test of association between a ma- amined the allelic composition of individuals trix composed of Nei’s unbiased genetic dis- within the overlap zone. The intermediate allele tancesamong individuals to a correspondingma- frequencies of localities within the overlap zone trix of the average taxonomic distances among are not due simply to combining in a single sam- thesesame individuals revealed a significant pos- ple individuals of both pure parental forms. itive correspondence(Fig. 4). The more dissim- Rather, some of the birds from these localities ilar two individuals are genitally the more dis- possessa mixed genie complement. In extreme similar they are morphologically. JULIA I. SMITH

TABLE 3. Number of individuals with particular al- .I . . lele combinations at ACON- and PGM loci for coun- . 2-4 . . . . . ties within zone of overlap. * 5-7 - >8 ...... :. ..:‘ ...... L1 Allelic composition of ACON-Z/PGM loci ...... “. . . . : .. . ._._.:.:.* . . . &.... :?‘...... _ . . CC/ BC/ BB/ BB/ BB/ DDI . . . .yi ’ ..:..*..i -..- 1‘ : . I._.’ ._ County CC CC CC BC CD CC ...... ~ . :...: .:I: . . :...... - ...... : ...... : .:: ...... Harmon 1 6 1 1 Cottle I 1 . . 8: ’ ^‘ .:::1.::.f:“%?‘ ::.~::::::~:::.z: . Williamson 2 2 2 . . . “...... “...... -...... :’ . . . . . * . ..:...;.x.:::: *:.:‘ :.: :::‘ .‘ :...‘ ...... ” ......

. . “.:~~c~:~‘ ::‘ “.:.::‘ ’ :. : . : ’ ......

......

i 0.5 1.0 1.5 2.0 25 leles indicates that southern Texas Golden-front- TAXONOMIC DISTANCE ed Woodpecker populations are genitally most FIGURE 4. Mantel test of covariation between Nei’s divergent from the Red-bellied Woodpecker unbiasedgenetic distance and average taxonomic dis- populations of central Oklahoma. Therefore, the tancesamong the same individuals (t > 6.5, P i 0.05, discovery of individuals within the zone of over- r = 0.415). lap with genie compositions that include the B allele at the ACON- locus (characteristic of the DISCUSSION Golden-fronted Woodpecker) and the C allele at My primary objective was to determine whether the PGM locus (characteristicof the Red-bellied Red-bellied and Golden-fronted woodpeckers Woodpecker) suggeststhat the woodpeckersare hybridize. On the basis of intermediate mor- interbreeding in the zone of overlap (Table 3). phology there is evidence that the two species Initially, I identified hybrids by the a priori interbreed. I identified 25 putative hybrids (four assumption that they would exhibit intermediate females and 2 1 males) that were collected within morphologies. There is a significant association or near the zone of species overlap. The fre- between morphometric and genie characteristics quency of hybridization is 15.8%, which is con- (Fig. 4); these two character setsdescribe similar siderably greater than the level (5%) reported for patterns of geographicvariation, which supports hybridization between Gila and Golden-fronted the identification of the 25 putative hybrids with- woodpeckers(Selander and Giller 1963). in the zone of overlap. The analysis of genie variation also supports Sexual selection may facilitate hybridization the identification of hybrids within the zone of between the two species. In particular, female overlap. In particular, the electrophoretic anal- Red-bellied and Golden-fronted woodpeckers ysis of 12 loci revealed a closegenie affinity; there may prefer mates with red napes. The napes of are no fixed allele differences between the two male Golden-fronted Woodpeckers are more red woodpeckers.Prager and Wilson ( 197 5) have re- than their female counterparts. Johnson and ported that avian pairs with many more genie Johnson (1985) have noted a related condition differencesthan Red-bellied and Golden-fronted in hybridizing sapsuckers which Howell (see woodpeckerscan still produce viable hybrids. Johnson and Johnson 1985) originally termed a The significant patterns of geographic differ- “lust for red.” Female sapsuckersare said to pre- ences in allele frequency support the conclusion fer males with red plumages. Kilham (196 1) re- that the two speciesare interbreeding in the con- ported a comparable situation in which a female tact zone. Golden-fronted Woodpeckersare most Red-bellied Woodpecker in captivity persistent- common in south Texas and Red-bellied Wood- ly solicited toward a female Pileated Woodpeck- peckersare most numerous in central Oklahoma. er (Dryocopus pifeutus) perhaps prompted by its The significant local patterning of PGM and extensive red crest. Similarly, female Golden- ACON- alleles indicates that geographically fronted Woodpeckers may preferentially select closesouth Texas populations of Golden-fronted red-naped mates, resulting in the extensively red Woodpeckers are also genitally similar (Table 2, and orangenapes of male Golden-fronted Wood- Fig. 3). Likewise, geographically close Red-bel- peckers. However, in the area of overlap the lied Woodpecker populations of central Okla- completely red napes of male Red-bellied Wood- homa are genitally very similar. By contrast, the peckerswould present to female Golden-fronted significant regional patterning of these same al- Woodpeckers a “super stimulus” and could lead WOODPECKER HYBRIDIZATION 385 to hybridization. This hypothetical female pref- CarnegieMus. Nat. Hist., and the Univ. Okla. Stovall erencemay promote hybridization between these Mus. Ron Ennel-Wilson collected a relativelv large number of the specimensused in this study. The Texas two species. Parks and Wildlife Game Division and the Oklahoma If two species do not meet, they cannot Department of Wildlife Conservation provided co- hybridize. Range extension resulting in an operationand assistance.I am gratefulto Michael Smith, increased area of sympatry thus increases the Peter Stangel,and the staff of the SavannahRiver Ecol- probability of hybridization. In the recent past ogy Laboratory for their assistanceand supportof my research.The electrophoreticanalyses were supported Golden-fronted and Red-bellied woodpeckers by contract DE-AC09-76SR00819 between the U.S. appear to have extended their ranges in south- Department of Energyand the University of Georgia’s western Oklahoma. The area of overlap between Institute of Ecology. My research was supported by Golden-fronted and Red-bellied woodpeckers grants from: Frank M. Chapman Memorial Fund of the American Museum; Alexander Wetmore Memo- corresponds, in part, to an ecologically inter- rial Fund of the American Ornithologists’ Union; So- mediate area where xeric southern conditions ciety of Sigma Xi Grants-in-Aid of Research,Univer- meet mesic northern habitats. The influence of sity of Oklahoma Department of Zoology; and the environment upon the distributions of these Oklahoma Biological Survey. I thank Danial Hough two species is unknown. Hamilton (1962) has for assistancewith computer analyses. Bruce Miller furnished materials for the analysisof plumage color. argued that speciesdistributions within ecolog- Field assistancewas provided by James-Krup< Jenella ically intermediate areas are determined pri- Love. Leslie Nitikman. and StenhenSecor. Regina Ma- marily by environmental limitations. He sug- cede provided assistancewith illustrations.I thank Mi- gested that taxa become trapped within these chael Mares, Doug Mock, and Gary Schnell for sug- gestionson early draftsofthis manuscript.I am indebted biotically intermediate zones unable to adapt to to Gary Schnell for his guidance and generosity the prevailing conditions on the other side. This throughout the course of my study at the University implies that in southwesternOklahoma there has of Oklahoma. This work was completed in partial ful- been an amelioration of environmental condi- fillment of the requirements for the degree of Master tions that has promoted the range extension of of Scienceat the University of Oklahoma. Golden-fronted and Red-bellied woodpeckers. In contrast, Selander and Giller (1963) have ar- LITERATURE CITED guedthat the Golden-fronted Woodpecker,which BENT, A. C. 1939. Life histories of North American has adapted to a wide variety ofhabitats through- woodpeckers.U.S. Natl. Mus. Bull. 174. out its extensive range, has the evolutionary po- DYKSTERHUIS.E. J. 1948. The vegetationofthe West- tential to occupy much of the eastern range of em Cross Timbers. Ecol. Monogr. 18:325-376. the Red-bellied Woodpecker. They concluded HAMILTON.T. H. 1962. The habitats of the avifauna of the’mesquite plains of Texas. Am. Midl. Nat. that competition with Red-bellied Woodpeckers, 67:85-105. rather than environmental composition, limits HARRIS,H., ANDD. A. HOPKINSON.1976. Handbook the extent of range overlap. This implies that for of enzyme electrophoresis in human genetics. the extent of overlap between these two species North-Holland Publishing Co., Amsterdam. JOHNSON.N. K.. AND C. B. JOHNSON.1985. Snecia- to change, as it apparently has in southwestern tion in sapsuckers(Sphyrupicus): II. Sympathy,hy- Oklahoma, there must have been a change in bridization and mate preferencein S. ruberdugetti their comnetitive interactions. Therefore. it would and S. nuchalis.Auk 102:l-l 5. be of value to investigate this area of apparent KILHAM, L. 1961. Reproductive behavior of Red- bellied Woodpeckers.Wilson Bull. 73:237-254. range expansion for recent ecological changes, as MAYHEW,D. A. 1983. A new hybrid cross,Notropis well as modifications of woodpecker behavior atherinoides x Notropis volucellus(Pisces: Cy- that may have developed and could account for prinidae), from the lower Monongahela River, the increased sympatry in this region and sub- western Pennsylvania. Copeia 1983:1077-1082. sequent increasedopportunity for hybridization. MAYR, E. 1970. Populations, speciesand evolution. Harvard Univ. Press. Cambridee. MA. ACKNOWLEDGMENTS MOORE,W. S., AND D. B. BLJCHANA~‘1985. Stability of the Northern Flicker hybrid zone in historical I thank the curatorsand staff of the following museums times: Implications for adaptive speciationtheory. who loaned study skins: Natl. Mus. Nat. Hist., Am. Evolution 39:135-151. Mus. Nat. Hist., Univ. Kansas Mus. Nat. Hist., Texas MUNSELLCOLOR. 1970. Munsell limit color cascade. COOD.Wildl. Collections. Louisiana State Univ. Mus. Munsell Color Co.. Baltimore. MD. Zooi., Univ. Michigan Mus. Zool., Delaware Mus. Nat. NEW, N. A., AND G. R. SMITH. 1979. Multivariate Hist., Field Mus. Nat. Hist., Midwestern State Univ., analysisof hybrid fishes. Syst. Zool. 28: 176-196. Peabody Mus. Nat. Hist., Baylor Univ. StreckerMus., NEI, M. 1978. Estimation of average heterozygosity 386 JULIA I. SMITH

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