Hybridization Between Bombina in Slovakia and Hungary

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J.evol .Biol. 1:3-14(1988) 1010-061X/88/01 0003-12 $1.50 +0.20/OQ 1988 Birkhiuser Verlag, Bawl

Hybridization between the fire-bellied toads Bombinabombina and Bombina variegata in the karst regions ofSlovakia and Hungary: morphological and allozymeevidenceGiinter Gollmann ,x3 Petr Roth*, and Walter HijdlKey words: Hybrid zone; allozymes; Bombina bombina; Bornbina variegata;amphibia.

AbstractGeographic variability and genetic interactions in the contact zone between thefire-bellied toads, Bombina bombina and B. variegata, were studied using analysis ofmorphological and genetic variation in sixteen samples from the Slovak Karst and

Aggtelek Karst regions. Genotype frequencies at four marker loci (Ldh-1, Mdh-2,Adk, Hem) demonstrate the existence of a hybrid zone with highly variable popu-lation structures. While some samples appear to represent panmictic hybrid popu-lations, other samples are very heterogeneous. Pure individuals of both speciesoccurred together with hybrids at one site. Habitat segregation among geneticallydifferentiated demes probably causes this heterogeneity of population structures.Increased frequencies of the allele Ldh-l, which is present in low proportion inB. bombina south of the contact zone, were found in some hybrid populations.

IntroductionThe analysis of natural hybridization is one of the central and most active fields inthe study of speciation. Conjectured dynamics of hybrid zones are of great impor-

Institut fiir Zoologie, Universitat Wien, Althanstr. 14, A-1090 Vienna, A ustria CS-277 21. Libechov 84, Czechoslovakia3 Present address: Department of Zoology, University of Melbourne, Parkville, Victo ria 3 052, Austra lia

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4 Gollmann et al.tance in several pertinent hypotheses, including the classical assumption of rein-forcement of premating reproductive isolation (adaptive speciation theory sensuMoore and Buchanan, 1985) as well as the theories of parapatric and stasipatric spe-ciation (Endler, 1977; White, 1978). Two decades ago it was a widely accepted opi-nion, termed the ephemeral-zone hypothesis by Moore (1977), that zonal hybridi-zation was a short-lived phenomenon which would eventually lead either to fusion ofthe hybridizing taxa or to perfection of isolating mechanisms (see Wilson, 1965;Remington, 1968). However, more recent studies have produced ample evidenceindicating that many hybrid zones are apparently stable and of ancient origin (seeMoore, 1977; Barton and Hewitt, 1985). Explanations for this stability have beensought along three main lines of argumentation:

a) Hybrids are less fit than both parental forms; hybrid zones persist owing to abalance between dispersal and selection against hybrids. Hybrid zones maintainedby this mechanism have been termed tension zones (Key, 1981; Barton andHewitt, 1985).b) Hybrids have greater fitness than either parental form in a restricted ecotonalregion.c) Different alleles are selected for in different environments on both sides of ahybrid zone.Moore (1977) and Moore and Buchanan (1985) contrasted the first two models as(a) dynamic-equi librium hypothesis and (b) bounded hybrid superiority hypo-thesis, emphasizing the differences in selective regimes (endogenous vs. exoge-nous) thought to be crucial in determining the fitness of the hybrids.

The hybrid zone between the European fire-bellied toads, Bombina bombina andB. variegata, has already been studied by electrophoretic analysis of allozyme mar-kers in some parts of Central Europe (Szymura, 1976a, b; Gollmann, 1984,1986, inpress; Szymura and Barton, 1986). Characteristic features of this hybrid zone are itsgreat length and a considerable variation in population structures among differentgeographic regions. The position of the zone is clearly related to environmental fac-tors and distinct adaptations of both species: B. variegata inhabits hil ly and moun-tainous areas and usually spawns in small, intermittent pools, while B. bombina is alowland species breeding in larger, more permanent bodies of water.

In an investigation on distribution and hybridization of both species in Slovakia,utilizing only morphological methods, Lac (1961) reported a peculiar situation fromthe Slovak Karst area: The lowland form B. bombina lived on the plateau of Silica(Silicka planina) at higher altitudes than B. variegata, which was found in the neigh-bouring valley of the river Slana. Lac (1961) suggested that the warmer climate of theplateau, in connection with recent human activities, would create favourable condi-tions for B. bombina.This paper presents a new investigation of the fire-bellied toads from the SlovakKarst area and adjacent parts of Hungary (Aggtelek Karst), studying both morpho-logica l and allozymic variation. A preliminary compilation of a part of these data hasalready been published (Gollmann, 1986). Here we give ful l details of the results,compare them with the findings of Lac (1961), and discuss their implications forsome general questions in the study of hybrid zones.


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Hybridization in BomhinaMaterial and Methods

A total of 176 specimens (82~Yd, 859 Q, 9 j uv was collected in August 1983)(Slovakia) and July 1984 (Hungary). Sample sites are indicated in the map (Fig. 1)and characterized in the following list. For each location name (usually that of anearby village), approximate altitude, sample size and a brief description of the habi-tat are given.

Fig. 1. Sample sites in the Slovak Karst/Aggtelek Karst region. Location R is situated 3.5 km south of theposition of the corresponding mark. Inset shows region (black rectangle) on a larger scale.


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6 Gollmann et al.A. Krasnohorska (300 m), n = 15, wheel rut puddles in Krasnohorska-Dlha Luka,immediately north of the bridge over river CremoSna.B. Jovice (280 m), n = 15, wheel rut puddles on a country road and a moderatelyvegetated ditch near Jovice, in agricultural land south of river CremoSna.C. Gombasek (260 m), n = 16, a pool above the curbed spring near Gombasek.D. Bohdnovo (210 m), n = 7, a stream about 1 km north of Bohunovo, in the sec-tion between its passage under the road from PleSivec to Bohuiiovo and where itjoins the river Slana.E. Silicka Jablonica (300 m), n = 10, shallow pools near Brezinovsky brook northof Silicka Jablonica.F. Silica I (580 m), n = 15, a fe w richly vegetated pools in a ditch about 600m east

of the lake JaStCrEie jazero. One specimen collected in a shallow puddle very close toJaSteri-ie jazero and another one, caught in a puddle on the road about 200 m east ofJaSterCie jazero, are also included in this sample.G. Silica II (500 m), n = 7, wheel rut puddles in a meadow beside the road, about1500 m east of locality J.H. Silica III (490 m), n = 11, a drainage ditch about 1 km southeast of Silica.J. Silica IV (500m), n = 8, the bank of a large pond about 500m southeast ofSilica.K. Silicka Brezova (500m), n = 15, hoofprint puddles at a spring in a dolina,about 1 km west of Silicka Brezova.L. Mines-volgy (270 m), n = 8, small puddles, a part of them with little flow, nearthe stream MCnes-patak.M. Dlha Ves (340m), n = 7, two drainage ditches in an agricultural cooperative inDlha Ves.N. Voros-to (320 m), n = 13, a large pond, vegetated with reeds and pond-weed.P. Imola (260m), n = 8, hoofprint puddles at a draw-well at Avas-oldal west ofImola.Q. Szolosardo (250 ), n = 11, a well southeast of Szoliisardo.R. Rudabanya (300 m), n = 10, a large pond north of Rudabanya, with reeds andpond-weeds growing close to the bank.Bombina tadpoles (including metamorphosing specimens) were observed at loca-tions B, F, G and M, juveniles were present at sites A, B, D, G, J and K.Colour pattern and skin structure characters were recorded using the classificationtables of Lac (1961) and Gollmann (1984). As both species exhibit considerableoverlap in morphometric relations, and because heterogeneity in the composition of

sex and size classes among the samples and small sample sizes would introduce addi-tional bias, no morphometric data will be given in this paper.Electrophoretic investigations followed standard procedures (see Gollmann,1984). Variation of the following proteins was studied: lactate dehydrogenase(LDH, EC 1.1.1.27), malate dehydrogenase (MDH, EC 1.1.1.37), creatine kinase(CK, EC 2.7.3.2), adenylate kinase (ADK, EC 2.7.4.3), phosphoglucomutase(PGM, EC 2.7.5.1), glucosephosphate isomerase (GPI, EC 5.3.1.9) and hemoglo-bin (HEM).


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Hybridization in RombinaResults

Results obtained by both morphological classification tables were in good agree-ment. The heterogeneity of several samples precludes meaningfu l comparison ofaverage values of populations, as presented in earlier papers (Gollmann, 1984, inpress). To allow direct comparison of morphological and electrophoretic data, indi-vidual values at a morphological character index (MCI), which is based on the fourcharacters that discriminate best between the two species (for details see Gollmann,in press), are indicated in the genetic hybrid index diagram (see below, Fig. 2).Detailed data on individual colour pattern variation are available on request fromthe first author.

Fig. 2. Distribution of individuals over the hybrid index (HI) in all samples. Values at the morphologicalcharacter index (MCI) are shown by shading of the rectangles representing single individuals: black =bombin a-like (O-2), ha tched = intermedia te (3-S), white = variegatu-like (6-S).

Electrophoretic phenotypes found in this investigation were the same as describedin previous studies (Szymura, 1976a; Gollmann, 1984, in press). The nomenclatureof loci and alleles follows these papers. Ldh-2 and Pgm were monomorphic for thesame alleles in al l samples, at Mdh-2 a few individuals showed variant patterns, thegenetic basis of which could not be unambiguously resolved. Allele frequencies at sixpolymorphic loci and average heterozygosity at these loci, determined by actualcounts, are given in Table 1. To examine the statistical significance of increased fre-quencies of the rare allele Ldh-lM in some hybrid populations (see also Fig. 4 anddiscussion) these data were checked against approximations, which were estimatedusing the assumptions of a normal distribution of alleles and a linear decrease of both


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Hybridization in Bomhitza 9bombina-alleles (Ldh-l, Ldh-1) with increasing shares of the variegatu-alleleLdh-lF across the hybrid zone. Frequencies of Ldh-lM were found to be significantlyhigher than the approximated values in samples H (a


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10 Gollmann et al.Slovako-Hungarian Karst region bombina-like populations were found, whichshowed decreasing frequencies of introgressed variegata-alleles towards the south(samples M, N, P, Q and R).These data require cautious interpretation, as sampling was carried out in latesummer after the main breeding period. Seasonal migrations of Bombina are known(see Madej, 1973; Beshkov and Jameson, 1980; Kapfberger, 1984), although notwell understood. Meteorological conditions causing fil ling or desiccation of pondsand puddles certainly affect these migrations strongly. The summer of 1983 wasexceptional ly dry. So, it is possible that many toads were not collected at their breed-ing sites; rather, individuals spawning at different places may have been concentrat-ed in a few remaining pools.

Fig. 3. Average frequen cies of bomb& -alleles (black sectors) at four (for sam ples A and B three) mar-ker loci.

Nevertheless, some conclusions on the structure of the contact zone in the SlovakKarst/Aggtelek Karst area can be drawn. Populations of almost pure B. variegatuand almost pure B. bombina are separated by a hybrid zone of about 20 km width(see Fig. 3), which is roughly the same as found in other parts of Central Europe (seeKaraman, 1922; Szymura, 1976b; Gollmann, 1984). But whereas in most other


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Hybridization in Bombina 11regions zones of allopatric hybridization (sensu Woodruff, 1973) exist, showingtransition of gene frequencies through sequences of panmictic hybrid populations instepped clines (Gollmann, 1984; Szymura and Barton, 1986), the genetic structureof the hybrid zone in the Slovako-Hungarian Karst area is more complicated. Pureindividuals of both species are present i n the centre of this zone, although extensivehybrid ization occurs. At some sites hybrid populations may have reached geneticequilib rium. Altitude is a poor predictor of gene frequencies in this area.

To explain the heterogeneity of population structures in this hybrid zone is a mat-ter of speculation. Habitat qualities are undoubtedly of great importance in deter-mining position and character of the contact zones in Bombina. The patchy environ-mental structure of the karst region creates possibilities for habitat segregationamong genetically differentiated demes. Thus, choice of different breeding placesmay account for the sympatric coexistence of both species in the presence of a majo-rity of hybrids.

The data given by Lac (1961) are too sparse to allow any valid inference onchanges in the hybrid zone in the course of the last 2.5 years. However, a retreat of B.bombina, as was observed in other parts of Slovakia (Gollmann, 1986), seems tohave taken p lace in this region, too.

A gloss on the rare allele phenomenonIncreased frequencies of otherwise rare alleles and the occurrence of unique

alleles in hybrid populations have been noted in many investigations of hybrid zones(see Case and Williams, 1984; Murphy et al., 1984; Barton and Hewitt, 1985; Kat,

Fig. 4. Frequencies of L&-Z alleles in 19 Bombina populations (Closed circles: data from this study; opencircles: hybrid populations from the Laborec valley in eastern S lovakia, see Gollmann, 1986) given asaltitudes of the triangle. The line close to the basis indicates the expected mean frequencies of allele M inhybrid populations assuming neutral diffusion.


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12 Gollmann et al.1986). Hunt and Seiander (1973) suggested that selective values of alleles may bealtered in the new genetic environment created by introgression. Other possibleexplanations for increased frequencies of minor alleles in hybrid populations includehigher mutat ion rates in hybrids (Woodruff and Thompson, 1980), intracistronicrecombination (Golding and Strobeck, 1983) and genetic drift (Szymura and Swies,1979). The small sample sizes of the present study are not well suited for detectingrare alleles or accurately determining their frequencies. However, the variation infrequencies of Ldh-lM allows some inferences to be drawn on this topic. This al lo-zyme obviously did not arise by mutation or intragenic recombination in the hybridzone, as it is present in B. bombina outside this zone, usually in frequencies of about10 % in northern Hungary (Szymura, in prep.; Gollmann, in press; locations N, P, Qand R of this study). It is striking that the highest frequencies of Ldh-lM are found inhybrid populations showing an intermediate genetic constitution (Table 1, Fig. 4).Sampling error and genetic drift may contribute to this pattern of variation, yet itseems to fit the assertion of modified selective regimes in hybrid populations betterthan a purely neutralistic interpretation of the rare alle le phenomenon.

Dynamics of hybridization in BombinaThe narrow hybrid zones in Bombina appear to be stable, even if their positionmay have been subjected to large changes during postglacial range expansion of both

species (Arntzen, 1978) and to smaller shifts in historical time. So far, no indicationsof either incipient fusion of the parental gene pools or of character displacementhave been found in any area of contact between B. bombinu and B. variegata.The many obviously adaptive differences between the two species (see Szymuraand Barton, 1986, p. 1142) suggest that differential selection of alleles on both sidesof the contact zone is a significant component in the dynamics of hybridization.Given the existence of intermediate habitats, this dissimilarity would also provide abasis for regarding a hybrid superiority model. However, increased embryonic mor-tality and a higher incidence of morphological aberrations in the centre of the hybridzone near Cracow lead Szymura and Barton (1986) to the conclusion that selectionagainst hybrids was the primary force in maintain ing this hybrid zone. Consideringthe pronounced local differentiation among hybrid populations in Lower Austria,Gollmann (1984) assumed that gene flow between these populations was unimpor-tant; like populations H (Silica III) and K (Silicka Brezova) from Silicka planina theypossibly represent stabilized hybrid swarms, which have regained genet ic balance ina process resembling the founder-flush model of Carson (1975; Carson and Tem-pleton, 1984). Circumstantial evidence from other vertebrate species shows that re-establishment of genomic coadaptation may indeed proceed rap idly in hybrid po-pulations (see Graham and Felley, 1985). Unfortunately, sufficient genetical andecological data on Bombina, which could allow a profound synthetic approach tointegrate these partly confl icting findings and ideas, are still missing.At best, a comparative assessment of geographic variation may provide someclues to the under lying mechanisms maintaining these hybrid zones. Modifications


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Hybridization in Bombinu 13of evolutionary interactions along contact zones have been detected in a number oftaxa (see Harrison and Arnold, 1982; Littlejohn and Watson, 1985; Howard, 1986).Various factors have been discussed n attempts to account for this variability: dura-tion of the contact, genetic variation in the hybridizing taxa, and variation in ecologi-cal conditions. In Bombina, neither the time which has elapsed since the first contactnor genetic variation in either speciescan explain the pattern of variation among dif-ferent parts of the hybrid zone; thus, population structures seem o be determined bylocal environmental conditions and by casual events during colonization of particu-lar habitats (Gollmann, 1984; Gollmann and Szymura, 1986; Szymura in prep.).The scope of the present study is restricted by small sample sizes and the limitednumber of electrophoretic markers and morphological characters that have beenanalysed. Nevertheless, it may hold asa general conclusion that even more elaboratemorphological and genetic investigations may help in sharpening questions on thedynamics and evolutionary significance of hybrid zones, rather than answeringthem. To achieve the goal of understanding these hybrid zones, detailed field studiesof behavioural ecology and population dynamics will be necessary.

AcknowledgementsWe thank 0 . Gy. Dely for advice on the Hungarian nature protection regulatio ns and J. Simko, Orsza-

gos Kornyezet- es Termesze tvedelmi Hivatal, Miskolc, for kindly issu ing colle ctio n permits for NorthHungary and the Aggtelek Reserve. We are indebted to J. M. Szymura and N. H. Barton for comm unicat-ing unpu blishe d data, and to J. W. Arntzen, J. M. Szymura, H. G. Tunne r and G. P. Wagner for critica llyreading an earlier version of the manu script. Th is research was funded by the Fonds zur Forderung derwissensch aftlichen Forschung, Wien (projects 4750 and 5445, granted to Prof. F. Schaller).

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339-345.Barton. N. H., and G. M. Hewitt. 1985. Ana lysis of hybrid zones. Ann. Rev. Eco l. Syst. 16: 113-148.Beshkov, V. A., and D. L. Jame son. 1980. Movement and abunda nce of the yellow -bellied toad Bombinavuriegutu. Herpetologica 36: 365-370.Carson, H. L. 1975. The genetics of speciation at the diploid level. Amer. Natur. 109: 83-92.Carson, H. L., and A. R. Templeton. 1984. Genetic revolutions in relation to speciation phenomena: the

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Hybridization Between Bombina in Slovakia and Hungary

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