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2005 Reproductive Success Across the Black-capped Chickadee (Poecile atricapillus) and Carolina Chickadee (P. carolinensis) Hybrid Zone in Ohio C. L. Bronson
Thomas C. Grubb, Jr.
Gene D. Sattler Liberty University, [email protected]
Michael J. Braun
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Recommended Citation Bronson, C. L.; Grubb, Jr., Thomas C.; Sattler, Gene D.; and Braun, Michael J., "Reproductive Success Across the Black-capped Chickadee (Poecile atricapillus) and Carolina Chickadee (P. carolinensis) Hybrid Zone in Ohio" (2005). Faculty Publications and Presentations. Paper 35. http://digitalcommons.liberty.edu/bio_chem_fac_pubs/35
This Article is brought to you for free and open access by the Department of Biology and Chemistry at DigitalCommons@Liberty University. It has been accepted for inclusion in Faculty Publications and Presentations by an authorized administrator of DigitalCommons@Liberty University. For more information, please contact [email protected]. The Aiik 122(3):759-772, 2005 © The Americiin Ornithologists' Union, 2005. ^L Printed in USA. REPRODUCTIVE SUCCESS ACROSS THE BLACK-CAPPED CHICKADEE {POECILE ATRICAPILLUS) AND CAROLINA CHICKADEE (P. CAROLINENSJS) HYBRID ZONE IN OHIO
C. L. BRONSON,' ' THOMAS C. GRUBB, JR./ GENE D. SATTLER,' AND MICHAEL J. 'Dqmrtiticnt of Evolution. Ecohi^y, and Organlsmal Biology, The Ohio Staff Uiiivcrsifii, 318 West Tllli AveiUK Columims, Ohio 43210. USA: 'Di-piut)Jiciit of Biolo;^y mid Cliemistri/, Libert]/ Uniz'crsity, 1971 University Boiilcvnrii, i\/mhbuy^, Vir^iniiJ 24502, USA; mid iciit ofVcrldinUe Zoolo;^y, Nntioiuil Miisciofi ofNntiirnl History, Siiiillisoniiin Institution, 4210 Silver tliil Roud. Siiiliand, Mmyhmd 20746, USA
CT. —Black-capped Chickadees (/'(ifc;7fi7fr;L"(7/)/7/i/s) and Carolina Chickadees (P. cawliueusis) hybridize in an east-west band from New Jersey to Kansas. Within the past century, the Ohio portion of this hybrid /one and the Carolina Chickadee range to the south have been moving northward, whereas the Black-capped Chickadee range has retracted. In Ohio, we characterized the genetic composition of the hybrid zone using five diagnostic molecular loci. Although there was no evi- dence of assortative mating in the center of the hybrid zone, we found a relative pau- city of genetically intermediate breeding females as compared with breeding males. That suggests viability selection against female hybrids, in line with Haldane's rule. On the basis of reproductive variables (number of nestlings, reproductive success), we found a decrease in productivity of breeding pairs in the hybrid zone that is significantly and positively related to their probability of producing homozygous offspring at each autosomal or sex-linked locus. We also found that the decrease in productivity was significantly and positively related to the genetic composition of the male of the pair {i.e. pure male chickadees more productive). These data strongly suggest that hybrids are at a selective disadvantage. Because the zone of reduced reproductive success was considerably narrower than the zone of introgression, our results demonstrate that genetic introgression is occurring in the face of substantial selection against hybrids. Received 16 April 2004, accepted W jmniary 2005.
Key words: Black-capped Chickadee, Carolina Chickadee, genetic indices, hybrid zone, Poecile iitricapillus, Poecile carolinensis, reproductive success.
Exito Reproductivo a traves de la Zona de Hibridacion de Poecile ntricapillus y P. carotiiicnsis en Ohio
RESUMEN. —Las especies Poecile atricapillus y P. caroliucnsis hibridan en una franja orientada de este a oeste desde New jersey hasta Kansas. Durante el ultimo siglo, la seccion de Ohio de esta zona de hibridacion y el rango de P. carolinensis al sur de esta se han desplazado hacia el norte, mientras que ei rango de P. atricapillus se ha contraido. En este estudio, caracterizamos la composicion genetica de la zona de hibridacion en Ohio usando cinco loci moleculares diagnosticos. Aunque no cxistio evidencia de apareamiento asociativo en el centro de la zona de hibridacion.
'Present address: Department of Internal Medicine, Division of Immunology, The Ohio State University, 473 West Twelfth Avenue, Columbus, Ohio 43210, USA. E-mail; bronson.3("osu.odti 759 760 BRON-ION Lr AL. [Auk, Vol. 122
encontramos una relativa carencia de hembras reproducHvas geneticamente intermedias en comparacion con los machos reproductivos. Esto sugiere la existencia de seleccion por viabilidad en contra de las hetnbras hibridas, lo que concuerda con la regla de Haldane. Con base en variables reproductivas (nt'imero de pichones, exito reproductivo), encontramos una disminucion en la productividad de las parejas en la zona de hibridacion que esta significativa y po.sitivamente rclacionada con SLi probabilidad de producir crias homocigoticas en cada locus autosomico o ligado a! sexo. Tambien encontramos que la disminucion en la productividad estuvo significativa y positivamertte relacionada con la composicion genetica del macho de la pareja (i.e. los machos puros fueron mas prodiictivos). Estos datos sugieren fuertemente que los hibridos se encuentran en desventaja seloctiva. Debido a que la zona de exito reproductivo reducido fue considerablemente mas estrecha que la zona de introgresion, nuestros resultados demuestran que a pesar de que existe seleccion en contra de los hibridos, esta sucediendo introgresion genetica.
ZONE ij-iNAMics is a fertile area for -100 km farther north, approximately along U.S. research on natural selection and speciation, Highway 30 (Grubb et al. 1994, Peterjohn 2001). because of the exchange of genes between In other words, the Black-capped Chickadee distinct groups (Harrison 1990, 1993; Hewitt distrihtition has been receding northward. 1988). Within birds (see review in Grant and The chickadee hybrid zone is quite narrow, Grant 1992), the hybridization of many North with genetic cline widths on the order of 20 American species has been studied (for review to 30 km (Sattler 1996, Sattler and Braun 2000). of Great Plains hybrid zones, see Rising 1983). Given the likely age of contact and the dispersal For example, Black-Capped Chickadees (Poecile capabilities ot chickadees (Weise and Meyer atricapillus) and Carolina Chickadees {P. caroli- 1979), the narrow cline widths suggest that ncnsis) are known to hybridize in many areas some sort of selection may oppose introgression along their common border (e.g. Kansas: across their hybrid zone {Barton and Gale 1993). Rising 1968; Missouri: Braun and Robbins 1986, In Illinois, Brewer (1963) found that hatching Sawaya 1990; Illinois: Brewer 1963; Ohio: Grubb success was lower in the chickadee hybrid zone et al. 1994; Virginia: Johnston 1971, Sattler 1996, than for either parental species, but he had Sattler and Braun 2000; West Virginia: Sattler complete data on only four hybrid zone nests. 1996, Sattler and Braun 2000; Pennsylvania: He attributed the reduction to infertility and Ward and Ward 1974, Cornell 2001). Because retarded development of eggs. these species may not be sister taxa (Gill et al. We wished to study the relationship between 1989, 1993; but see Sattler and Braun 2000 for hybridization and reproductive success in greater discussion), only limited hybridization might detail. The objectives here were to employ genetic be expected. markers to map one segment of the hybrid zone In North America, except for a peninsular in north-central Ohio and to examine the rela- distribution in the Appalachian MoLintains, tionship between genetic composition of the the Black-capped Chickadee distribution abuts parents and reproductive success. the north edge of the Carolina Chickadee di.s- tribution (Mostrom ct al. 2002). In the southern Appalachians, Black-capped Chickadees are often found at high elevations, and Carolina Field nicthods. —The area of the hybrid zone Chickadees at lower elevations. In the early studied within Ashland County, Ohio (4O''5O'N, 1880s, Carolina Chickadees were described as 82"15'W) was bounded by County Road 700 on permanent residents only within the southern the north. State Route 95 on the south. State portion of Ohio (Wheaton 1882). By the late Route 89 on the west, and County Road 175 on 1930s, the hybrid /one was probably located the east (Fig. 1). The study area was 23 km from acrt)ss the middle of the state, approximately in north to south and 6 km from west to east. The the location of the east-west U.S. Interstate 70 landscape was about equally divided among (Trautman 1940). Currently, the zone is located pasture, row crops, and woodlands. To limit the July 2005] clive Success in tli/hriii Zone 761 overlap of points in Figures 2-4, the 21 sampling In November of 1993 and 1994, we placed locations were condensed to 10 pooled s^imples remote-controlled Feeder traps (Pierce and based on similar latitudes. Frt>m north to south, Grubb 1979) filled with sunflower seeds within the groupings were a-b, c, d, e, g-f, h, i-m, n-p, privately owned woodlands af all study sites q-r, and s-u (Fig. 1). within the zone. From December through
CR700
5-
10-
km 15-
25-
FIG. 1. Tbe study transect (light gray area) in Ashland County, Ohio, indicating sampling points (letters) and major roadways. 762 BKONSON hi' AL. [Auk, Vol. 122
February, we trapped or mist-netted chickadees and Pst l/mtDNA) into a genetic index (Cl) visiting each feeder. In late February, we placed for each individual, calculated as tbe number artificial nesting snags (Grubb and Bronson of Carolina Chickadee alleles divided by tbe 1995) in the woodlands and monitored them total number of alleles examined (Bronson et al. through the chickadee breeding season (to the 2003). Tbere are two alleles for eacb autosomal end of June). marker and one for tbe mtDNA haplotype. Tbe At the time of capture, we banded each bird Z-linked marker has two alleles in males and with a federal aluminum band and a colored one in females (females are tbe heterogametic leg streamer (Sullivan 1984) tor individual sex in birds). Thus, Gl was hased on up to eight identification from a distance. We weighed marker alleles for females and nine marker eacb bird to the nearest 0.1 g using a spring alleles for males. For some of the nonparametric balance. Unflattened wing chord and tail length correlations, Gl was transformed were measured to tbe nearest 0.5 mm, and tar- sus length (from the hent "elbow" to tbe hent Gr = |GI-0.5| "wrist") to tbe nearest O.l mm. Sex was initially determined tbrougb bebavioral observation to adjust for the potential underlying parabolic subsequent to capture (i.e. males dominant to distribution of Gl. Transformed Gl' ranges from females) and relative size of tbe members of 0.5 for either pure Carolina Chickadee or pure a pair (Desrochers 1990, Smith 1991). Sex was Black-capped Cbickadee to 0 for maximal inter- later verified for many individuals on the basis mediate birds. of vocalizations (e.g. singing males, begging For each set of parents, a compatibility index females) and morpbology (e.g. male cloacal (Cl) was calculated on tbe basis of tbe expected protuberance, female brood patch). Finally, sex proportion of homozygous offspring tbey could was determined through genetic techniques produce at eacb autosomal or sex-linked locus, (see sex-linked marker below). averaged across loci (Bronson et al. 2003): Maleailnr nietlwtis. — Methods for collecting blood, extracting DNA, genetic analysis, and parental analysis are detailed in Bronson et al. (2003). Tbe genetic markers employed are wbere ^^ are the autosomal loci (fi, = Eco Rl/ski, diagnostic restriction-fragment-length poly- c^-, = B
We expected /; \iriori tbat several variables botb number of nestlings or fledglings (I-'ig. 3B) (all reproductive measures and Cl of a hreeding and reproductive success (Fig. 3C) displayed pair) would bave reduced values in tbe middle apparent troughs near the midway point of the of the hybrid zone. Consequently, for figures zone. The effect on reproductive output in those involving the relevant comparisons, a second- troughs appears to be substantial; at least half order polynomial trend line was included tbe eggs failed to batch in 14 of 22 nests between (instead of a linear trend line), but both types 5 and 15 km, whereas 0 of 7 nests outside tbat of lines are shown, if only to facilitate visual zone had batcbing success <0.7. However, tbose assessment ot the pattern. troughs were also narrow; all nests witb repro- ductive success <0.5 wore found in tbe region RLSULT.S from 7.4 to 13.0 km. For breeding individuals, Gl of eacb sex The frequencies of alleles at marker loci con- had a positive and significant relationship sistently changed in a clinal fasbion across tbe with location in the study landscape (female byhrid zone, from a low proportion of Carolina Gl: Spearman's p = 0.553, /' = 0.002, n = 29, Fig. Cbickadee alleles in tbe nortb to a bigh propor- 4A; male Gl; Spearman's p = 0.769, P < 0.001, tion in tbe soutb, witb the midpoint in allele II = 29, Fig. 4B). There was a paucity of breeding frequency between 10 and 15 km in all five cases females of intermediate Gl in comparison with (Fig. 2). Thougb coincident in position, some breeding males (e.g. no females vs. 12 males in variation among markers in dine width was the Gl range from 0.3 to 0.6; Fig. 4A-B). Tbe Cl apparent. For example, tbe frequency oftbe Pst 1/ of breeding pairs was lowest in the middle of C7 marker allele changed from 0 to 1 between the transect (Fig. 4C). That trough coincided 7.4 and Id.2 km, whereas Eco RMski only varied with tbe trough in productivity (Fig. 3C). from about 0.1 to 0.8 over the entire transect. Transformed Gl of tbe female ranged from Across tbe byhrid zone, we obtained records 0.12 to 0.50 (Fig. 5A-B) and was not signifi- of reproductive output for 29 pairs of chicka- cantly related to any reproductive measure dees. Tbere was no significant correlation (Table 2). Tbe lack of females (only one) with between genetic indices of tbe male versus a transformed Gl <0.25 could bave weakened female of each pair (Spearman's p = 0.310, P = the correlation. The transformed Gl of tbe male, O.IOI, /; = 29), wbich suggests that mating was which ranged from 0.05 to 0.50 (Fig. 5C-D), was nonassortative. Genetic confirmation of parent- not significantly related to clutch size (Table age for two nests could not be obtained, because 2), but was positively and significantly related of a laboratory accident that caused the loss of to number of nestlings or fledglings (Table 2; the DNA for tbe nestlings. We analyzed DNA Fig. 5C) and to reproductive success (ratio of fingerprints for the remaining 27 nests, finding fledglings to egg; Table 2; Fig. 5D). no evidence of extrapair fertilizations. Of tbe The Cl between tbe male and female of a 100 offspring tested, 14 had one or more unat- breeding pair ranged from 0.25 to 1.0 (Fig. 6). tributable bands. None of those 14 individuals Although Cl was not significantly related to could be excluded as tbe offspring of the puta- clutch size (Table 3), it was positively and signifi- tive parents on the basis of band-sbaring scores cantly related to number of nestlings or fledglings (Wetton et al. 1987). (Table 3; Fig. 6A) and to reproductive success For all 29 pairs, tbere was no loss of offspring (ratio of fledglings to egg; Table 3; Fig. 6B). between batching and fledging. Therefore, for those 29 pairs of chickadees, number of nestlings DISCUSSION equaled number of tledgUngs, fledging success (ratio of fledglings to nestlings) was lOO'fi., and St'iection and hybrid zone malnti'nance.—Our reproductive success (ratio of tledglings to eggs) results demonstrate tbat tbere is a narrow region equaled batching success (ratio of nestlings to of reduced reproductive success at the center of eggs) (Table 1). Figure 3 places various reproduc- tbe chickadee hybrid zone in Obio. We moni- tive measures within the study landscape (with tored a 23-km transect of the /one witbin wbicb a second-order polynomial trend line included we observed substantially reduced reproduc- for easier visualization). No trend was appar- tive output of populations in tbe center of the ent in clutch size across the zone (Fig. 3A), but transect as compared with tbose at eacb end. On 764 BRONSON ET AL. fAuk, Vol. 122
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North-south distance (km) North-south distance (km)
North-south distance (km)
FIG. 2. Distribution of Carolina Cbickadee alleles al eacb of five loci across tbe study site in nortb- ccntral Ohio. Kilometer 0 is Asbland County Road 700, tbe nortbern boundtiry of the study area. (A) EcoR Vski, II = 143; (B) Ava II/RI'7, u - 121; (C) Bgl 1I/RP104, n - 142; (D) Pst I/C7, ii = 60; (H) Pst 1/ mtDNA, n ^ 142. Only adults, not nestlings, were used for tbe analysis to limit nonindcpendence of data points because of relatedness. All available adults (breeders and nonbreeders) were included. Varying sample sizes are attributable to (1) difficulty in scoring a few nonbrceding individuals, especially for Ava TI/RP7; and (2) a need to know tbe sex of eacb individual to determine tbe num- ber of alieles to be considered for Pst I/C7. Consequently, only individuals observed breeding were included for tbat locus to insure tbe correct attribution of sex. tbe basis ot geograpbic distributions of allele area or for Carolina Chickadees in general, tbe frequencies for five diagnostic genetic markers, extremes of our transect bad a similar number tbe transect we monitored spanned tbe core of of Black-capped Chickadee fledglings to tbe tbe bybrid zone. Brewer (1963) also provided southern peninsula of Micbigan (5.5 vs. 6.6; anecdotal evidence of reduced reproductive Nickell 1956). Therefore, we are confident tbat success in the cbickadee bybrid zone. Altbougb the observed reduction in productivity is lim- comparable reproductive success data (tledg- ited to tbe bybrid zone and is not a widespread lings per successful clutch) are not available cbickadee phent)menon. Reduced reproductive for either Black-capped nr Carolina chickadees success indicates tbat some form of selection is in areas immediately adjacent to tbe study operative in the bybrid zone. July 2005] Rcjirodiictivc Success in Hybrid Zone 765
TABLE 1. Genetic and reproductive data for each pair of chickadees observed. All nestlings fledged. The location column gives the letter designation of each site (see Fig. 1) and its distance in kilometers from the northern end of the study transect.
Location Genetic index Reproductive variables Compatibility Km Site Female Male index Clutch Nestlings 1.1 a 0.125 0.111 1.000 4 4 1.1 a 0.250 0.222 0.750 7 5 3.4 c 0.125 o.m 0.875 8 8 7.0 d 0.000 0.111 0.875 8 6 7.4 e 0.750 0.333 0.625 7 3 7.4 e 0.000 0.444 0.500 7 2 7.4 c 0.125 0.778 0.250 7 6 9.8 f 0.250 0.000 0.625 9 1 9.8 f 0.250 0.222 0.875 5 4 9.8 g 0.000 0.333 0.625 7 2 9.8 8 0.000 0.444 0.625 6 2 11.5 h 0.125 0.333 0.625 8 1 12,2 i 1.000 0.333 0.375 8 5 12.2 i 0.125 0.556 0.375 8 3 12.2 i 0.875 0.556 0.625 8 2 12.2 i 0.125 0.778 0.500 7 5 12.2 k 0.750 0.222 0.500 8 4 12.2 1 0.625 0.333 0.375 7 1 12.2 1 0.875 0.333 0.375 7 1 13.0 n 0.750 0.444 0.500 7 3 13.0 n 0.000 O.f)67 0.375 6 1 13.0 n 0.000 0.667 0.375 8 7 13.0 o 0.750 0.556 0.625 6 3 13.0 o 0.250 0.667 0.375 4 4 13.0 P 0.750 1.000 0.750 6 5 16.2 q 1.000 0.889 0.875 7 7 16.2 r 1.000 1.000 1.000 9 9 22.4 t 1.000 1.000 1.000 7 7 22.4 u 1.000 1.000 1.000 7 6
What is the nature of selection in tho chicka- precipitation) also could have been involved. dee hybrid zone? Reduced reproductive success Although we did not detect any gradients or was linked to genetic intermodiacy of males and other inconsistencies in environmental char- to the genetic compatibility of a breeding pair. acteristics across our sample transect, such Those links suggest that intrinsic genetic incom- exogenous factors (Harrison 1990, Arnold 1997) patibihties are responsible for the reduced could have existed and been causal. Because of reproductive success. However, although its observational nature, our study cannot dif- reproductive measures were related to genetic ferentiate between intrinsic or extrinsic factors characteristics of the breeding pairs, both repro- in the reduced reproductive success. ductive measures and genetic characteristics The best method for separating those causes were also related to geographic position within is to perform a manipulative experiment the zone (Fig. 3). Thus, parental genotypes (Moore and Price 1993). Therefore, as a may not have been an exclusive cause for the result of the observations reported here, we reduced productivity in the middle of our relocated chickadees of bolh parental species sample transect. For example, environmental atid hybrids into isolated island woodiots attributes (e.g. food availability, temperature. within the hybrid zone and again observed 766 BRONSON ET AL. |Auk, Vol. 122
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FIG. 4. Relationship of genetic and compat- North-south distance (km) ibility indices of breeding individuals with location in the hybrid zone. Kilometer 0 is Ashland County Road 700, the northern bound- Fic. 3. Relationship of reproductive variables ary of the study area. The four sizes of circles with location in the hybrid zone {with the from smallest to largest indicate sample sizes of second-order polynomial trend line for easier 1, 2, 3, and 4, respectively. (A) Female genetic visualization). Kilometer 0 is Ashland County index; (B) male genetic index; and (C) compat- Road 700, the northern boundary of the study ibility index of breeding pair, including the area. The four sizes of circles from smallest to second-order polynomial trend line for easier largest indicate sample sizes of 1, 2, 3, and 4, visualization. The CI is calculated as the pro- respectively. (A) Clutch size, (B) number of portion of Carolina Chickadee alleles present nestlings or fledglings, and (C) reproductive in an individual {0 = Black-capped Chickadee; success (ratio of fledglings to eggs). 1 = Carolina Chickadee). The Cl was calculated using the average of the proportion of homozy- gous offspring a breeding pair could produce at each of the loci (0 = least compatible; 1 = most compatible). Julv 20051 Rcpwductizv Si(ft"fss i)i Hybrid Zone 767
B
Transformed genetic index of female Transformed genetic index of female
m • 09' D
0 7 •
OB
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Transformed genetic index of male Transformed genetic index of male
FIG. 5. Relationship of reproductive variables with transformed genetic indices, and linear trend lines for easier visual comparison. The four sizes of circles from smallest to largest indicate sample sizes of 1, 2, 3, and 4, respectively- (A) Number of nestlings or fledglings versus female GI', Spearman's p = 0.305; (B) reproductive success (ratio of fledglings to egg) versus female GI', Spearman's p = 0.229; (C) number of nestlings or fledglings versus male GI', Spearman's p = 0.579; (D) reproductive success (ratio of fledglings to egg) versus maleGI', Spearman's p =0.540. TheGr(Gr = IGl -0-^1) is calculated from the proportion of homozygous allele pairings present in an individual (0.5 = Black-capped or Carolina Chickadee; 0 = maximal intermediate birds).
T.\B].r 2. Spearman's rho (p) ft>r chickadee reproduction on the transformed genetic indices (GI' = IGI - 0.51) of the female and male of a pair. Sample size for all correlations is 29, Significant relationships based on the sequential Bonferroni technique (/i^^,. = /' x [4 - Rank]; Hochberg 1988} are shown in bold.
Sex Reproductive variable P P Rank Padi Female Clutch size 0,076 0-696 3 0.696 Nestlings or fledglings 0.305 0.107 1 0-321 Reproductive success 0.229 0.231 2 0.462 Male Clutch size 0.165 0.391 3 0.391 Nestlings or tledglings 0.579 0.001 1 0.003 Reproductive success 0.540 0.002 2 0.004
reproductive success (Bronson et al. 2003). greater reproductive success than hybrid pairs The results of that experiment indicated that similarly moved within the zone. Thus, with endogenous factors are primarily responsible the environment held relatively constant, the for selection in the Ohio section of the observed reproductive decline of hybrids in chickadee hybrid zone. When pure pairs were the hybrid zone must be mainly attributable to moved into the hybrid zone, they still had intrinsic genetic factors. 768 BRONSON F,T AL. |Aiik, Vol. 122
Selection in fhe zone is probably balanced by inward dispersal of naive parentals to cre- ate a stable, narrow hybrid zone (Barton and Hewitt 1989). A variety of evidence suggests that this hybrid zone is temporally stable (e.g. Tanner 1952, Rising 1968, Robbins et al. 1986, Grubb et al. 1994, Sattler and Braun 2000; but see Merritt 1981). The habitat in which these chickadees meet lacks obvious barriers and has been relatively unchanged since the last glacial maximum, so it is plausible that the hybrid zone Compatibility index of breeding pair existed long before it was detected. There is no evidence of assortative mating in our data or in previous studies (Robbins et al. 1986). Also, all 1.0 1 • • i 0.9 genetic clines in this and previous studies of the IgOB hybrid zone (Sawaya 1990, Sattler 1996, Sattler d> and Braun 2000) were coincident in position, u at o and dine widths were generally narrow with 10 06 0) respect to the dispersal capabilities of chicka- > 05 3 04 dees (Weise and Meyer 1979). All these facts suggest that a narrow hybrid zone has existed a * between these chickadees for a relatively long «02 IT 4 period, and that a balance of selection and dis- 01 • 1 B persal maintains the zone. 00 Compatibility index of breeding pair Both the demonstration of intrinsic selec- tion against hybrids and the recent northward FIG. 6. Relationship of reproductive variables movement of the zone are indications fhat this with CI of breeding pair, and linear trend portion of fhe chickadee hybrid zone functions lines for easier visual comparison. Small, as a "tension zone" (Key 1968, Barton and medium, and large circles indicate sample Hewitt 1985). In such cases, the location of the sizes of 1, 2, and 3, respectively. (A) Number zone reflects a balance between dispersal from of nestlings or fledglings. Spearman's p = 0.425; parental populations and selection against (B) reproductive success (ratio of fledglings individuals of mixed ancestry, regardless of to egg). Spearman's p = 0.450. The CI was environment. The zone then moves until it calculated using the average of the proportion reaches a location limiting either popula- of homozygous offspring a breeding pair could tion density or dispersal (Harrison 1993). produce at each of the loci (0 = least compatible; Tension zones are believed to be one of the 1 = most compatible). most common kinds of hybrid zones in nature (Barton and Hewitt 1989). Caveats.—The CI used here and bv Bronson et al. (2003) is one of a suite of possible compat- ibility indices. Our CI considers each available
TABLE 3. Spearman's rho (p) for chickadee reproduction on the cumpaHbility index of the breeding pair. Sample size for all correlations is 29. Significant relationships based on the sequential Bonferroni technique (^i^j =p ^ [4-RankJ; Hochberg 1988) are shown in bold.
Reproductive variable Rank Clutch size -0.027 0.888 0.888 Nestlings or fledglings 0.425 0.021 0.042 Reproductive success 0.450 0.014 0.042 July 20031 Reproductive Si 1922, Orr 1997, Turelli 1998). An analysis of fhe comparison, the patterns of introgression in nestling sex ratio in the chickadee hybrid zone the genetic markers across a zone also provide in Pennsylvania yielded a lack of significant information about the strength of the barrier, support for Haldane's rule (Cornell 2001). Our because they represent the long-term effect of data relating to fertility also show no support hybridization. When hybridization is effective for fhe rule; the observed reduction in produc- (i.e. backcrosses are presenf), a hybrid zone is tivity was related to male genetic composition, less analogous fo a wall and more like a semi- not female. It should be noted, however, that permeable membrane that allows alleles to pass the small number of genetic markers employed through at various rates, depending on allele- could have contributed to the difference in the specific selection factors (Barton 1983). relationships of female GI and male CI wifh reproductive measures. Male GI had a larger ACKNOWLEDGMENTS number of possible values because of the inclu- sion of a sex-linked marker. We thank many woodland owners for Haldane's rule may not directly apply to allowing us to work on their property; S. comparisons of parenfal genetics with repro- Humrichouser for his untiring help with field ductive measures in all cases. Reproductive work; N. Arguedas and C. Huddleston for variables such as hatching success should be assistance with lab work; and R. Curry, S. compared to the sex of the offspring themselves. Gaunt, F. Gill, D. Nelson, P. Parker, the Ohio Unfortunately, we do not know the sex of nesf- State Universify (OSU) Behavioral Ecology Hngs or unhatched eggs. If viability is affected, Group, the Smithsonian Laboratory of Haldane's rule would predict an increased ratio Molecular Systematics lunch group, and three of females to males in unhatched eggs with a anonymous reviewers for discussion and com- compensatory decrease in the ratio for viable ments. This study was funded by the American offspring. Ornithologists' Union (Betty and Herbert Carnes Other data from the present study indicate Award) and American Museum of Natural thaf there may be a viability effect on females. History (Frank M. Chapman Memorial Fund) fo For example, a distinct gap between 0.3 and C.L.B., and was performed under OSU ILACUC 0.6 exists in the distribution of adulf breeding- protocol 93A0206, federal banding permif 20653, female GI (Fig. 4A). By confrasf, 12 males had and Ohio banding and collecting permit 509. GIs between 0.3 and 0.6 (Fig. 4B). Apparently, highly heterozygous females had been removed LITERATURE Cirpn from our population samples before reproduc- tion, the sampling point of this study. Therefore, ARNOLD, M. L. 1997. Natural Hybridization and Haldane's rule might well have been manifested Evolution. Oxford University Press, New by reduced viability of females prior to repro- York. ductive age. BARION, N. H. 1983. Multilocusciines. Evolution Conclusion.— Our results indicate that the 37:454-471. width of the zone based on reduced reproduc- BARTON, N. H., AND K. S. GALE. 1993. Genetic tive success (-6 km) is less than half that based analysis of hybrid zones. Pages 13-45 in on the genetic indices (>15 km). Furthermore, Hybrid Zones and fhe Evolutionary Process this relationship of reproductive and genetic (R. G. Harrison, Ed.). Oxford University indices of hybridization is likely conservative, Press, New York. because we know that two components of GI BARTON, N. H., ANDG. M. 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