Analysis of Hybrid Zones Author(S): N

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Analysis of Hybrid Zones Author(s): N. H. Barton and G. M. Hewitt Reviewed work(s): Source: Annual Review of Ecology and Systematics, Vol. 16 (1985), pp. 113-148 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/2097045 . Accessed: 07/06/2012 18:39

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ANALYSIS OF HYBRID ZONES

N. H. Barton Departmentof Genetics and Biometry, The Galton Laboratory,University College, London NW1 2HE, England

G. M. Hewitt School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, England

INTRODUCTION

Hybrid zones are, roughly speaking, narrow regions in which genetically distinctpopulations meet, mate, andproduce hybrids. They areoften only a few hundredmeters wide and yet may be severalhundred kilometers long. They are found in a wide variety of organisms:Tables 1 and 2 list about 150 reasonably clear examples, in which there is a spatial transitionbetween two hybridizing forms. Such a widespreadand strikingphenomenon requires explanation; more importantly,it offers us several ways of understandingthe natureand origin of species. First, hybrid zones pose interestingquestions for the taxonomist, for they contrasttwo views of the species: as a set of populations delimited by genetic barriersto gene exchange; and as a set of populationsmaintained in a particularstable equilibriumby selection. Second, the wide rangeof genotypes found in a hybrid zone can be used to analyze the genetic differences and selective forces thatseparate the taxa involved. This may allow some inferences aboutthe way these differences evolved and, by extrapolation,about the way fully isolated species diverge from each other. Finally, models of parapatric speciation, and of Wright's "shiftingbalance," involve the formation, movement, and modification of hybrid zones. Hybrid zones must be understood before the plausibility of these models can be judged. After clarifyingour terminology, we will summarizethe relevanttheory and then see how this can be used to make inferences from field data. A notable increasein the numberof detailedgenetic studiesof hybridzones occurredover 113 114 BARTON& HEWITT the last decade, and so our emphasis will be on the analysis of zones in nature. In this article we will only briefly mention their close relation with speciation and the "shiftingbalance."

TERMINOLOGY Species Biological species are "groupsof actually or potentially interbreedingnatural populationswhich arereproductively isolated from othersuch groups"(160, p. 120). If "reproductivelyisolated" groups are defined to differ genetically in such a way that they cannot exchange genes, then Mayr's definition is un- ambiguous.However, the widespreadoccurrence of stablehybrid zones has led even the originatorsof the biological species conceptto qualifytheir reliance on gene flow. For example, Mayr (163, p. 285) statesthat "the two species in such a case seem to remain'reproductively isolated' in the sense thatthey do not fuse into a single population"[see also Dobzhansky(69, p. 354), Grant(96, p. 51), Wright (273, p. 5), and Bigelow (35)]. Taken to its logical conclusion, this leads to what might be called the "coadaptive"species concept, in which species are the "incarnationof harmoniouswell-integrated gene complexes" (161, p. 295). We thinksuch a definitionundesirable, for threereasons: (a) The objectivityof the biological species stems from the requirementthat gene flow be completely absent;(b) we cannottell from contemporaryevidence whether two taxa will eventuallyfuse together;and (c) the persistenceof differences in particularcharacters despite gene flow is due to the effect of those characterson fitness, ratherthan on any featuresof the whole population(132, p. 439; 21, p. 134). For example, the butterflies Heliconius erato and H. melpomene are subdividedinto a series of strikinglydifferent mimetic races, each surrounded by a narrowhybrid zone. However, these races need not differ at more than a few genetic loci, and genes may flow freely between them;the races should not be given the statusof species because of the way selection acts at these few loci (247). We will thereforeuse gene flow to refer to the flow of neutralalleles, undistortedby selection, and reproductive isolation to mean "lack of gene flow" (132, p. 458). If two populations are to belong to different biological species, reproductiveisolation must be complete: No fertile hybrids can be formed (132, p. 455). Hybrid Zones Much variety of meaning has stemmed from confusion about the nature of "hybrids." The high proportion of hybrids within hybrid zones has often seemed surprising(e.g. 9, 100) and has caused hybrid zones to be defined as "narrowregions containing only hybrids, and separatingthe parentalforms" (35; see also 214). However, "hybrids"will inevitably be abundantif many ANALYSIS OF HYBRID ZONES 115 independent genes, or characters, are involved, simply because so many combinationsare possible. The term hybrid can also be misleading because it suggests thatthere is a single hybridphenotype, rather than the usual wide range of recombinants(see section below on Inference: Does Dispersal Maintain HybridPopulations?). We will thereforetry to base our discussion on genotypic frequencies, rather than on the crude dichotomy between parental and "hybrid." Many have restrictedthe termto dines formedafter the secondarycontact of two divergentpopulations (e.g. 161, p. 369; 214; 35; see 267). However, it is hardto distinguishprimary from secondarycontact without historical evidence (75, 267); more important, although a dine may have been set up after secondary contact, the differences may have originated within a continuous habitat(see section below on Inference: Primary or Secondary Contact?). Although some definitions restrict the term hybrid zone to narrow dines (161, 132) or, alternatively,to dines involving many characters(implicitly, 35, 74, 214, 267), it has often been appliedto chromosomaland mimetic dines defined throughone or two differences (e.g. Podisma pedestris, Warramaba viatica, Keyacrisscurra, Heliconius eratolmelpomene,Zygaena ephialtes; see Tables 1 and2 for references),and to dines muchwider than the likely dispersal of the organism (e.g. Thomomys,Lepomis). Endler (74, pp. 4 and 12) has defined a hybridzone as a "steepdine [with]increased variability of fitness and morphologybeyond that due to mixing and other randomeffects." However, most dines maintainedby selection will show increased genetic variance in fitness. Endler may be referringto the environmentalvariance seen in some hybridzones (74, p. 14; see also the section below on Rare Alleles in Hybrid Zones). In the bulk of the literature,a hybrid zone is synonymous with a cline. We would like the term to be used more precisely and have previously applied it only to dines maintainedby a balancebetween dispersaland selection against hybrids(15, 24, 114). However, we fear that the term is by now irretrievably confused, and so we will use it here simply to refer to a cline: that is, to a gradientor set of gradientsin morphologyor gene frequency, at one or more loci. Tension Zones We will arguethat most of the phenomenareferred to as hybridzones arein fact dines maintainedby a balancebetween dispersaland selection againsthybrids. These have several distinctive features. In particular,because they are not maintainedby a response to local environmentalconditions, they can move from place to place (15, 30, 130-132). Because they tend to move so as to minimizetheir length, Key (130) has termedthem "tensionzones"; we will use this term throughout. 116 BARTON& HEWITT

THEORY Maintenance of Clines Models of dines in continuoushabitats fall into two classes (180, Ch. 5). In the first class, dispersal is negligible. Selection maintainsa stable equilibriumat each locality [for example, throughheterozygote advantage(74, p. 64)]. The dine mirrors a smooth gradient in selection coefficients and hence in the equilibriumpoint. We will call these dispersal-independentlines; they include Moore's (170) "bounded hybrid superiority." In the second class, the homogenizing effect of dispersal is balanced against some cause of spatial heterogeneity.Most theoreticalwork has been on such models (74, 78). They include neutral lines, in which an initially steep gradientdecays with time; waves of advance of an advantageous allele (84); and dispersallselection balance, in which either differences in environment(107) or selection against intermediategenotypes (heterozygotes or recombinants)(30-32) maintainsa stable cline. We will refer to the last type as a tension zone. The distinctionbetween these two classes dependson the characteristicscale of selection, 1, where 1iVY, o2 = dispersal rate (more precisely, the variancein distancebetween parent and offspring), s is proportionalto selection or, for a neutral cline, the inverse of the time since contact (223). Any dispersal-dependentdine has a width (w, defined as the inverse of the maximum gradient)of the same orderas 1. For example, Bazykin (30) shows that a heterozygote disadvantages gives w = \/ 1. Conversely, if selection is to maintaina dispersalindependent cline, w must be much greaterthan 1. A dine can still be regarded as a dispersal/selection balance even if some hybrid genotypes are favored, provided they are only favored within a region much narrowerthan 1. When (as is usual) many dines coincide, linkage disequilibria will be generatedby the dispersal of parentalcombinations of alleles into the center (149, 224). If many genes are involved and selection is comparable with recombination,disequilibria will induce a sharpstep in each cline, flanked by long tails of introgression(Figure 1; 20). The central region of the dine (in which disequilibriaare strong) will be distinct from the surroundingtails, and its width will dependstrongly on the ratiobetween selection andrecombination (20). Movementof Hybrid Zones

MOVEMENT OF CLINES The factorsdetermining the movementof most sorts of dine are straightforward.Alleles involved in a dispersal-independentcline, or in a balance between dispersal and spatially varying selection, will rapidly spreadinto their equilibriumpositions. When dines at different loci overlap, theireffect as barriersto gene flow will pull them together(132, 224). Advanta- ANALYSIS OF HYBRID ZONES 117

bombina variegate

-R=0 5-) c 0 - 20Km Figure 1 Electrophoreticvariation across the hybridzone between the toads Bombina bombina and B. variegata near Cracow (237, and J. M. Szymura and N. H. Barton in preparation).The uppergraph shows the averagefrequency (p) over five diagnostic loci. The lower graphshows the averagepairwise linkage disequilibrium in each sample, relativeto the averageheterozygosity (R = LJ1pq). geous alleles will come to spread at constant speed, behind a sharp wave of advance (84, 234). In the case of neutral intergradation,the dine will lie wherever the two divergent populations first met.

MOVEMENT OF TENSION ZONES Tension zones can be moved from place to place by a variety of forces. These can be divided into those due to individual fitness, to population structure, and to the effects of gene frequencies on populationstructure. First, there are the effects of fitness differences between individualswithin local populations. One might expect the zone always to move in favor of the fitterallele. However, movementsdo not depend only on the relative fitnesses of the populations on either side of the zone ('180, pp. 217-233; 203). For example, in zones maintained by disruptive frequency-dependentselection (e.g. those between Mullerian mimics in Heliconius, or between coiling morphs in Partula), the dominant allele will tend to spread (155). Second, if density (p) or dispersalrate (u2) vary, or if dispersalis anisotropic, then therewill be a net flux of genes. This flux will push tension zones towards regions of low neighborhoodsize, or in the preferreddirection of dispersal(30, 82, 132, 183). For example, any tension zone will move at a speed au2(p,/p) down a density gradientp' (15). Since populationstructure is usually highly heterogeneousin nature(132, p. 451), tension zones are likely to be trappedby local barriers.They will move slowly, hopping from one local equilibriumto another, and so are more likely to be moved by large, sustained changes in populationstructure (in the extreme, extinction and recolonization)than by the steady effects -of asymmetricselection ( 15). Tension zones will, as their name suggests, move so as to minimize their length. Local bulges will be smoothed out by the greaterflux of genes pushingin fromthe convex side of the bulge (15, 118 BARTON& HEWITT

130, 132). The joint effects of curvatureand density gradientsare illustratedby the chromosomalhybrid zone in Podismapedestris (Figure2; 186). The zone is held in two places by inhospitableslopes and, in between, bulges out underthe pressureof the higher density on the easternside. This pressureis counterbal- anced by the tension of the zone. Finally, both density and dispersal may depend on gene frequencies; this seems especially likely for zones with strong effects on survival (e.g. alterna- tive mimeticpatterns in Heliconius, or pelage color variantsin Thomomys),and for hybrid zones involving many characters(e.g. Mus musculus/domesticus, Bombinabombinalvariegata). As well as a possible reductionin density within the "hybrid sink" (see below), there may be differences between the populations on either side. The type with higherdensity or dispersalwill spread;if the populationis rathersubdivided, so thatthe zone is trappedby local barriers, the analogous process is spread through differential rates of extinction and recolonisation (135, 144, 271). These three forces can all be absorbedinto a potential, which tends to a local maximum. This has the form H = -fN2dl + fF dA, and is a generalizationof the potentialderived by Barton( 15; see 29), whereN is neighborhoodsize (see below); 1is length, measuredrelative to the local width, which may vary;and A is area enclosed, again relative to local width. The first term, analogous to a "surfacetension," describesthe tendency of the zone to move to regions of low neighborhoodsize and to minimize its length. The second term, analogousto a 'pressure,"includes all the forces thatcause one type to advanceat the expense

< 1Km-

Figure 2 The position of the chromosomaldine in the grasshopperPodisma pedestris nearSeyne in the Alpes Maritimes, superimposedon the populationdensity (I186).The left and right dotted lines show the 10%and 90% frequencies of the chromosomalfusion, and the solid line the 50% frequency. The density contours are plotted at intervals of 0.5 adult grasshoppersm-2; solid shading indicates maximum density. The zone rests close to its predicted position (see text). ANALYSISOF HYBRIDZONES 119 of the other.H is a functionalof the complete configurationof the zone; the rate of movement (ax(l)lat) is proportionalto the gradient of H [u2aH/ax(l)]. No simple relationexists between the way the tension zone moves and either individualor populationfitness. Although H is a close analogue of the mean fitness, W, it is not identicalto it; mean fitness does not increasein a population subdividedby tension zones, unless one redefines fitness to equal H and so to includethe effects of gene flow andpopulation regulation. This makes it hardto interpretthe competitionbetween adaptivepeaks in Wright's"shifting balance" (271, 274) as a purely adaptive process. Barriers to Gene Flow

BARRIER STRENGTH In a continuoushabitat, the flux of alleles throughthe populationis proportionalto the gradientof allele frequency:the steeper the gradient,the greaterthe flux. When a flux of alleles meets a local barrier(either physical or genetic), a sharp step will build up. The size of this step is proportionalto the gradient,and so the barrierstrength can be measuredby the ratio between the step size and the flanking gradients (B = Au/u'; 183; see Bombinaexample below). B has the dimensionsof distance;it can be thoughtof as the length of unimpededhabitat that would presentan equivalentbarrier to a neutralallele. However, a local barrierhas very differenteffects on the flow of different sorts of allele. Although a moderatelystrong barrier,equivalent to a few hundreddispersal distances, may delay neutralalleles for tens of thousands of generations[V(B/u)2], even weakly selected alleles (s = 1%) may still flow past with a negligible delay of only a few hundredgenerations {- log [(B/ u)2Ts/s2]12s}(14, 27).

TYPES OF BARRIER Gene flow may be impededin threeways. First, environ- mentalfactors may reduce density or dispersal;the strengthof such a physical barrieris w(NI/N )2, where w is its width, and (NeIN(.)is the ratio between the neighborhoodsizes at the edge and at the center [N = 4rpa2, where p is the population density (272)] (N. H. Barton, in preparation). Although such physical barriersare not caused by genetic factors, they may be associatedwith tension zones, since these will move towards regions of low density and low dispersal (see above). Second, gene flow may be impeded by a reduction in density due to the lower fitness in a dine maintained by dispersal/selection balance. This has been termed the "hybridsink" effect (17, 108, 278); genes flow in from either side and are eliminated in the maladaptedindividuals at the center. This effect will only be importantwhen populationsize is sensitive to fitness, i.e. when selection is "hard"(256), and when overall selection is strong: B = w (We/Wc)2IR,where W is the mean fitness, andR = dlnW/dlnpis the strength of density-dependent regulation (17, and N. H. Barton in prepara- 120 BARTON & HEWITT tion). In Podismapedestris, the density of hatchlingsat the centerof the zone is abouthalf thatin purepopulations living in matchedvegetation (186; cf 16, 25). However, the densities of adults are indistinguishable;since most dispersalis by adults(26), the "hybridsink" will have little effect on gene flow, despite the strong selection against hybrids. In general, it is hard to see that the "hybrid sink" could often be comparable with the drastic direct effects of physical barriers. Finally, gene flow will be impededby associationsbetween alleles. To flow past a cdine, a neutralallele must recombine into the new genetic background before it is eliminatedby selection against the alleles with which it is initially associated(14, 34, 195, 231, 240). The barriercaused by an arbitrarypattern of mutilocus selection is approximatelyW(We/WC)2/r (20, N. H. Barton in preparation;N. H. Barton, B. 0. Bengtsson, in preparation),where r is the harmonicmean recombinationrate between the selected and neutralloci. We can see from this formulathat to producea strongbarrier (B > a; see above) the clines involved should be wide (w > a), the fitness at the center should be low (W,

ASYMMETRY Barriers to gene flow may be asymmetric, allowing more genes to pass in one direction than the other. Asymmetry may be caused by differences in fitness, differences in population structure, or by dine movement;these are hardto disentangle. We would expect more gene flow into the less fit population. Genes flowing into that population will be associated with alleles from the fitter population and so will be selected against less strongly than will genes flowing in the opposite direction. However, if one genetic equilibrium confers greater fitness, it may advance, displacing the alternativeequilibrium. As it moves forward, alleles from the region occupied by the inferiorequilibrium will be swept into the advancinggenotype, causing genes to flow in the directionopposite to thatexpected for a static zone (24, 27, 33, 173). In nature, tension zones will be trappedby local gradients in density or dispersal.Flow into the less fit populationis then counteractedby flow into less dense regions, rather than by dine movement. However, since we would usually expect similar average neighborhood sizes over the broad areas on either side of the zone, we would expect the net flow to be into the less fit population. ANALYSIS OF HYBRID ZONES 121

Modification of Hybrid Zones The ideas thatpremating isolation will evolve to reinforcepostmating isolation between hybridizing populations, and that charactersmay diverge so as to reduce competition, have long been promoted (67, pp. 155-58; 255, pp. 173-84; 69; 83, pp. 129-3 1). Reinforcementand characterdisplacement have been popular more because they allow species differences to evolve as an adaptiveresponse to hybridizationand coexistence, thanbecause of any strong evidence for their importance(see below). This enthusiasmhas strongly in- fluenced the neo-Darwinianview of hybrid zones: it has been thought that tension zones would be unstabletowards reinforcement and characterdisplacement, so that zones must eitherbe ephemeral,or are not maintainedby hybrid unfitness (e.g. 69, 170, 199, 266). Hybridzones may be modified in manyways andin unpredictabledirections. In zones maintainedby a balance between dispersal and selection, reduced dispersal, reduced selection against hybrids, and toleranceof a wider range of environmentswill all be favored (11; 83, pp. 127-28; 92). However, we will concentrateon modifiers of the mating system, largely because most of the literatureconcerns them. Paterson (190, 191) has argued that reinforcement is unlikely, because mating systems involve a delicate coadaptation between male and female componentsand so are hard to change. However, mating systems have often evolved in spectacularways; indeed, hybridzones often involve differences in courtship(22 out of 31 well-studied zones) and so contain the sort of variation thatmight form the basis for reinforcement.In any case, coadaptationdoes not imply stasis (54; see Lande's model, describedbelow). Still, unless the mating system is highly labile, changes are likely to be selected against outside the hybrid zone. If changes were advantageous,they would probably arise first outsidethe narrowzone. The disadvantageof modifiersmight be absolute-for example, if a change in matingcall increasespredation (e.g. 248)-or it might only apply when the new type is rare-for example, the rarertype might take longer to find its preferredmate (cf 171). Such a selective disadvantagewill preventmodifications diffusing away from the hybridzone and so changingthe rest of the species (as envisaged by 50, 69). This does not in itself preventthe eventual formation of isolated and coexistent species; as soon as the loss of fitness throughhybridization inside the zone becomes small enough, relativeto differences in resource use, the zone will collapse into broad sympatry. [Of course, this may never happen:Two competing species may remain separated in "ecological parapatry"(132, p. 432).] However, the evolution of modifiers within the zone may be preventedby the swamping effect of gene flow from outside: It can be shown that only modifiers causing a substantialincrease in (say) assortmentcould evolve (24, Figure7.4). Furthermore,any modification must depend on the limited variationin the narrowzone (67, pp. 209-10). We must now consider the genetic details of "modifiers."One may imagine 122 BARTON & HEWITT such parametersas dispersal, selection, and recombinationbeing modified rathersimply, by the increase of an allele at a single locus within the zone. However, where the mating system is concerned, it seems more likely that differentalleles must be establishedon either side (see 79). Most models have supposedthat prematingisolation is caused by alternativealleles at one locus thatis not itself subjectto naturalor sexual selection:That is, assortmentcauses no direct change in allele frequencies (50, 65,-79, 158, 249). Alleles at the assortinglocus may then become associatedwith those at the selected locus, or loci, thus increasingreproductive isolation. For this to occur, the loci must be linked sufficiently tightly, and substantialassortment must be produced (50, 79, 249). However, assortmentwithout sexual selection is implausible:If the rarerallele suffers a disadvantage,reinforcement is impeded(171; see above). Indeed, such systems will themselves maintain stable tension zones. Many other models might be considered. For example, consider a male character subject to both naturaland sexual selection, the latter resulting from female preferencesthat evolve throughtheir correlationwith the male character(83, 138, 142; 187, Ch. 8). Lande (143) has shown that here a dine maintainedby naturalselection will be steepened by sexual selection, and isolation will be increased. Thus, the reinforcementof mating isolation does not necessarily make tension zones less stable. All the models discussed so far involve only one or a few characters.Most hybrid zones involve selection on many genes (see below). If a modifier can gain an advantagethrough its effects on a large proportionof these genes-for example, by reducingthe overalldispersal rate-it can evolve moreeasily. This is because dines are much wider when selection is spreadover many loci; more modifiers will arise by mutationwithin the zone, and there will be less gene flow from outside. However, if a modifier only affects one or a few genes or characters,it is not clear how reinforcementmay be affected (see the corresponding section on Inference below). In summary, hybrid zones may, in principle, be modified in a variety of ways. However, there are many constraints,particularly on the reinforcement of mating isolation. These arise from the swamping effects of gene flow, the lack of variationwithin narrowzones, the need for tight linkage, and modifiers with substantialeffects, andthe complicatingeffects of sexual selection. It may be that when conditions allow ready modificationwithin hybridzones, evolution of the mating system outside the zone will be even faster.

INFERENCE Does Dispersal Maintain Hybrid Populations? Before we can make any detailedanalysis of a hybridzone, we must know how it is maintained.The primaryquestion is whetherintermediate populations are producedby selection alone, or by both dispersaland selection. This distinction ANALYSISOF HYBRIDZONES 123

dependson the width of the dine relativeto the characteristicscale of selection, I = ca/Y. Moore (170) has argued that in many vertebratehybrid zones, dispersal is indeed negligible, and that hybrids are instead favored in narrow ecotonal regions. This explanationcannot be excluded for a few cases (most often in plants:96, 233), wherehybrid populations are apparentlyisolated from one or both parents. However, our survey includes few such cases, since we view hybrid zones as fairly continuous transitionsbeween distinct forms. A purely selective explanationmay also be plausiblefor dines that are very wide comparedwith dispersal, and where it is known that selection is moderateor strong. For example, the hybrid zone between the gophers Thomomysbottae and T. umbrinusin the Sangrede Cristo mountainsis 200 km wide, compared with a dispersalrange thoughtto be less than 1 km in a generation(104). Yet, these taxa differ considerablyin karyotypeand pelage color. These characters are strongly correlated within populations, which (discounting pleiotropy) implies strong linkage disequilibrium,and hence strong selection. Many other dines seem wider than might be expected from a dispersal/ selection balance [e.g. Caledia captiva, Mus musculus/domesticus,Podisma pedestris, Urodermabilobatum, Bombina bombinalvariegata;see Figure 6.2 in (74), and Figure 3]. For example, both laboratorycrosses and linkage disequilibriashow that strong selection is acting against hybrids between the Moretonand Torresian races of Caledia captiva. If the zone remainsabout 350 m wide because of a balancebetween dispersaland selection, dispersalmust be at least 40 m in a generation(18). This is much greaterthan the rate of 5-10 m suggested by Shaw (211). The explanation is probably that these winged grasshoppersmove furtherthan this rate suggests (C. Moran, D. D. Shaw, personalcommunication). Dispersal measurements are usually underestimates; in particular, some long-distance migration, and occasional extinction and recolonization, may greatly inflate dispersal (see M. Slatkin, this volume). A dine in a polygenic character(for example, hybrid inviability) may be much wider than would be expected from the total selection acting (e.g. 25). In general, exceptinga few extremecases such as Thomomysbottaelumbrinus, the frequently excessive width of hybrid zones may be accounted for by high dispersaland/or the involvementof many genes. Given our usual ignoranceof dispersal and selection, the mechanisms maintaininga dine cannot be safely deduced by comparingits width with the characteristicscale. One would expect a dine maintainedin directresponse to selection to vary in width and in shape much more than one maintainedin a dispersal/selection balance (129). Hybridzones do often vary in width (e.g. Podisma pedestris, Bombina, Mus musculus/domesticus),and Moore (170, p. 268) has used this fact to supporthis model of "hybridsuperiority." However, such variations may be accounted for in many ways, even if the dines are maintainedin a dispersal/selectionbalance-by variationof dispersaland density with terrain, by genetic differentiationwithin each taxon, or by variations in degree of C oc r- k 'I) ct t

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Table 2

Taxon Ref. Taxon Ref Taxon Ref.

Accipiter 198 Erebia 154 Peromyscus 10, 49, 133, 206, 207, 225 Acomys 251 Fundulus 176 Alouatta 137a Galbil/a 101 Petrogale 42 Ambystoma 196 Gasterosteus 106 Ph/llodactylus 137 Anolis 146 Geocrinia 91 Phytomyza 39 Anopheles 44 Geomvs pc Picoides 216 Anser 60a Gerbillus 252 Pinus 167 Astrapia 164 Gryllus 112 Pipilo 219a Batrachoseps 253 Gvmnorhina 46 Plethodon 73, 115, 116 Bolitoglossa 254 pCa Heliconius 155, 247 PC Podisina 110, 113, 114 Bombina 93, 238 PC Hyalophora 59 Proechimus 90 Bufo 77, 97, 98 H/la 166 Pseudophryne 165, 268 Caledia 58, 174, 211 Icterus 61, 201 Pteroglossus 101 Campylorhynchus 210 Jaera 147 Pycnonotus 220 Cebus 137a Juniperuts 188 Quiscalus 275 Celeus 215 Kalotermes 236 Ramphocelus 219 Cepaea 123, 126 Kevacris 113, 131 Rana 6, 86, 117, 139, 140, 151, 205 Ceratophyllus 200, 250 Larrea 120 Cerion 94, 268 Lanius 189 Ranidella 45, 36, 37 Chilocorus 2 2 9, 2 7 7, Lepoinis 5 Rhus 276 278 Chorthippus 48 Limenitis 197 Sceloporits 109, 121, 222 Clarkia 40 Lunnodvnastes 152 Siginodon 88, 279 Cnemidophorus 68, 280 Litoria 150. 153 Silene 156 Colaptes 172. 212 Macrowtls 100 Sorex 3, 85, 87, 209 PC Corvus 60 Manmola 41 Spal/a 184, 185, 252 Crotaphytus 168, 169 Mwcrohl/a 38 Sperinophilits 62, 105, 181 Cryptocephalus 12 Morabinae 132 Sph 'rapicuts 125 Culmacris 132 MIis 1, 51. 52, 81. Steliella 71 119. 204. 230 Daphoenositta 218 Sturnella 145 Dendroica 13 Mvgalopsis 66 Thotnotnv's 104. 193. 194, 226, 227, 228, 242, 243 Desinognathits 128 Natrix 244. 245 pC Did'vnuria 64 Notropis 72 Tritirits 127, 208 pC

Drosophila 53 Ovis 182 Warrainaba 4, 113, 177. 178, 263, 264 Diplodactylus 137 Papio 89 Enneacan thits 95 Parda/otes 217 Urodermna 99, 103 Ensatina 43 pC Partlda 56 57. 1 22, Vermnivora 213 124, 179 Zonotrichia 8, 111 Parnis 68a Zvgaena 246 Perognathus 118, 192

a Table 2 is the main reference list (drawn from Literature Cited) of key papers selected from the often considerable literatureon each genus The numbersand proportionsof zones with variousattributes quoted in the text are derived from this total literature.Some informationcomes from personal communications(pc) for which we are grateful. Anyone wanting detailed references on any zone should write to one of us We would be pleased to learn of zones not listed ANALYSISOF HYBRIDZONES 129

18 23 13 ,' 6' 00 7 10OKm 260 0 08O-' 0, ,0

10 23 232 17 0 wo0 01 , , s ~~~~19,25 ox,

T 1Km ,,o 2 023 width/ 10M , width dispersal(O-)

10M lKm 10OKm Figure 3 The width of various hybrid zones is plotted against corresponding estimates of dispersal. The upperand lower dotted lines show the widths that would be maintainedby selection against heterozygotesof 10'- and 10', respectively. Dispersal estimates are often approximate and may be averages of a wide range of published values. I Bombina, 2 Caledia, 3 Cepaea, 4 Cerion, 5 Chorthippus,6 Colaptes, 7 Corvus, 8 Dendroica, 9 Gerbillus, 10 Grvllus, 11 Helico- nius, 12 Hyalophora, 13 Lepomis, 14 Maniola, 15 Mus musculusldomesticus,16 (deleted), 17 Natrix, 18 Peromvscus, 19 Pinus, 20 Podisma, 21 Sorex, 22 Spalax, 23 Thomomys,24 Warrama- ba, 25 Zonotrichia, 26 Zvgaena. modification. It seems unlikely to us that the only region where hybrids are favored should be a long, narrow strip; "hybrid superiority"should give a broken, patchy distribution. In contrast, most well-studied zones divide the species' range into the quilted patternexpected for tension zones (e.g. Warra- maba viatica, Podismapedestris, Heliconius erato andH. melpomene,Bombi- na bombinalvariegata, Thomomysbottae). Furthermore,in the absence of physical barriers, transects through hybrid zones usually follow either the smooth, sigmoid curves expected from single-locus models, or the stepped dines expected from genetic barriers(e.g. Podismapedestris, Bombinabombi- nalvariegata, Caledia captiva, Mus musculus/domesticus;Figure 1). The most powerful evidence comes not from geographic distributionbut from genotypic distribution.With dispersal-independentclines, one or a few hybridgenotypes would be favored, and so dines at differentloci would not be closely parallel. Yet, in all cases where different electrophoreticalleles are found on eitherside of the cline, hybridpopulations are highly polymorphicfor these alleles, and, apart from four of five cases (Geocrinia, Ambystoma, Clarkia,Sorex, and perhapsPeromyscus) , these dines are closely parallelwith each other and with morphological and chromosomalchanges (Figure 4). 130 BARTON& HEWITT

So, although hybrid zones are often wider than expected for a dispersal/ selection balance, this patternis best explainedby underestimateddispersal and multilocus effects. Both geographic and genotypic patternsfit with a balance betweendispersal and selection, and not with any form of "hybridsuperiority." In many cases, of course, there is direct evidence of selection against hybrids (see below). DispersallSelectionBalance: The Strength of Selection If a dine is maintainedby dispersaland selection, the strengthof selection can be inferredfrom the ratiobetween its width andthe varianceof parent-offspring distance:s cx(U/w)2. The precise relationdepends on the way selection acts, but an orderof magnitudeestimate can be made withoutknowing such details. (For a neutralcline, the figure is inversely proportionalto the time since secondary contact [lIT = 2-(ul/w2).] The dispersalrate, u, is only known well enough to use this relationin a few cases (Table 1). For example, in Podismapedestris (a flightless grasshopper), several mark-releaseexperiments (26, 186) and the pattern of spatial correlation of chromosomal and elecrophoretic polymor- - phisms (23, andN. H. Bartonet al, in preparation)give u 20 m gen.- 1/2. So, the selection maintainingthe chromosomaldine at its width of 800 m must be weak: = 0.5%. This is consistent with direct measurements of meiotic nondisjunction(< 1.6%)(16). However, the difficultiesof measuringdispersal make this a laborious method. Better estimates can come from linkage disequilibria. In simple models of multilocus dines (20, 224), such associations between alleles are expected to be producedby dispersal(see above) and, indeed, are found in most studies of hybridzones that would be powerfulenough to detect them (Table 1). If, as is usual, the loci are unlinked, strong disequilibriaimply strong selection and correspondinglyhigh dispersal (19, 20; J. M. Szymura & N. H. Barton, in preparation). The most direct informationcomes from measurementsof fitness. Evidence of selection has come from laboratorycrosses (e.g. Podisma, Caledia, Bombi- na), observationsof viability or fecundity in the field (e.g. Podisma, Partula, Pseudophyryne),or by comparisonof differentage classes (e.g. Rana, Notro- pis). Such methodscan usually only give approximatemeasures of fitness, and negative results (e.g. Colaptes) cannot rule out the presence of substantial selection. There may be less directevidence-e.g. coiling directionin Partula suturalis, mimetic patternsin Heliconius and Zygaena, the effects of chromosomal heterozygosity,or morphologicalaberrations (see section below on Rare Alleles in Hybrid Zones). Direct study of fitness complements the indirect methodsdiscussed above:The formergives the total selection pressureacting in the zone, whereas the latter give the selection on individual loci (see section below on Number and Types of Genes). ANALYSIS OF HYBRID ZONES 131

DispersallSelection Balance: Mode of Selection A dine may be set up, in oppositionto dispersal,in variousways: by the contact of distinct populations, by the advance of an advantageousallele, by spatial differences in fitness, or by selection towards alternativeequilibria. These processes, and especially the last two, are hardto distinguish. All single-locus models give essentiallythe same sigmoid dine shape (129). Morefundamental- ly, even if genetic differences initially evolve in response to environmental differences, epistaticinteractions may eventuallybecome the main force maintaining the hybrid zone (55, 74); for a dine to be maintained entirely by environmentalheterogeneity, selection must act independentlyon each locus. Sometimes, there may be direct or circumstantialevidence of selection against hybrids (see previous section), or in response to environmentaldifferences. The narrownessof the zone, combinedwith historicalevidence, often rules out neutralintrogression, or a wave of advance. Usually, however, one must fall back on indirect arguments. Since the main difference between tension zones and dines maintainedby spatiallyvarying selection is in the way they move, we might look for correlationsbetween the position of the hybrid zone and either environmentaldifferences or populationstructure. The arguments here are similar to (though less powerful than) those used above to find whether dispersal is important.In general, one would expect a more broken pattern if the distributiondirectly reflects environmentalheterogeneity. For example, the hybridzone between the chromosomalraces of Podismapedestris runs along the high ridge of the Alpes Maritimes;it is hardto believe that the varied and mountainousterrain south of this ridge constitutes an environment uniformly favorable to the southern form. Locally, there is no correlation between the zone andvegetation ( 186);instead, the distributionis accountedfor by variationin populationdensity, as expected for a tension zone (Figure 2). However, there is usually some correlationwith an environmentalgradient (24, 75). In some cases (17%; e.g. Podisma, Sorex, Cepaea, Alpine and AppennineMus, andHeliconius) such a correlationseems unlikely, thoughone cannot be ruled out. Hybridzones may run parallelto climatic gradients(e.g. Caledia, Mus musculus/domesticus,Natrix, Corvus), vegetation differences (e.g. birdhybrid zones in the GreatPlains, Sceloporuswoodi), or differencesin soil type (e.g. Warramabaviatica, many gopher zones). Such associations must, however, be interpretedcautiously. They do not imply that most zones are maintained by an independent response of each character or allele to environmentalgradients. Tension zones will tend to move towards the point where the two forms are equally fit; moreover, the expansion of two populations into secondary contact may run parallel to environmentalgradients. Thereis often a broadenvironmental association, but no close relationwith any gradient (e.g. Caledia, Spalax, Rana pipiens, Icterus galbula, Sceloporus grammacus).Moreover, hybrid zones areoften found at local physical barriers, 132 BARTON& HEWITT which would not usually be expected for an environmentallymaintained dine [e.g. Caledia at the MaryRiver, Spalax (58/60 chromosomeraces), Podisma]. A second indirect argumentis based on the close coincidence of dines at differentloci. Unless all the relevantenvironmental variables are concentrated in a sharp ecotone (not usually the case), dines should be scattered. (The attractioncaused by linkage andthe "hybridsink" effect will be negligible if the dines are more than one width apart.) In contrast, many processes will make tension zones clump together (see section above on Movement of Hybrid Zones). The closely parallelpatterns found in almost all hybridzones (Figure4, see above) argue strongly for the importanceof hybrid unfitness.

a/ ~~~~by

0*~~~~~~~~

Pi . 0 0 0

C 0 ~~~~dy

P~~~~~~~

p- >

Figure 4 Graphsof the frequency(p,) of diagnosticalleles at differentloci (i), againstthe average frequency over all loci (15),across four hybrid zones. If the dines coincide precisely, the points would all lie on the diagonal. a) Bonbina, (5 enzymes), b) Urodermna,(3 chromosomalfusions), c) Rana, (6 enzymes), d) Mus, west Jutland, (3 enzymes). ANALYSISOF HYBRIDZONES 133

Thus, several argumentsconvince us that a substantialproportion of hybrid zones, and a majorityof the betterstudied zones, are tension zones maintained at the interface between alternativeequilibria. There is often direct evidence that hybrids are less fit; it is hard to imagine how selection would act independentlyon many loci; geographicdistributions suggest thatenvironmental gradientsare importantin determiningthe position of hybridzones but do not show what maintainsthem; and the usual concordanceof many charactersis inconsistent with maintenanceby spatially varying fitness. Primary or Secondary Contact? There has been great interestin the question of whether dines have arisen by primaryor secondary contact (e.g. 55; 67, pp. 207-10; 75; 83, pp. 125-31; 262). However, this question must be split into two components:whether the original differentiation arose in an essentially continuous population, and whetherpresent-day hybrid zones arose throughsecondary contact. Only the first componentis relevantto models of speciation, but only the second can be addressedby currentobservations (74, 75). The issue is furtherblurred by the difficulty of distinguishing,even in principle, primaryfrom secondaryorigin. Changesmay arise within small isolates embeddedin the centerof the species' range [162; see Hewitt (113) and Key's (131) discussion of Warramaba viatica]. Conversely, if a populationis divided into two allopatricbut extensive regions, changes must still arise in parapatrywithin these regions. Most of the zones in Tables 1 and 2 could be accounted for by secondary contact, usually since the last glaciation: 37% are clear examples. In Europe, and much of North America, few hybrid zones could have survived such climaticfluctuations; even in areasthat were not glaciated, such as the Amazon basin, climaticallyinduced range changes may accountfor the presentdistribu- tions of manytaxa (102, 246). It has been suggestedthat human disturbance has allowed contactbetween previously disjunctgroups (2; 7, pp. 138, 195, 474). While this may explain many cases of sporadic hybridizationbetween plant taxa, we feel that most hybrid zones are more ancient. There is rarely much historicalevidence as to the stability of hybrid zones, and what little there is goes back a centuryat most (e.g. Bombina, Colaptes). Some hybridzones are known to have moved rapidly (e.g. Bufo, Corvus, Icterus, Quiscalus, Tritur- us). Since it is hardto see how strong selection could cause rapid concordant changes in many characters, these cases are most likely due to population expansion. More often, hybridzones are known to have been essentially static for millenia:for example, threechromosomal races of Warramabaviatica meet on KangarooIsland in South Australia(263). The hybridzones between them extrapolateout to those on the mainlandand so must have been in the same position since the island was cut off from the mainland8,000-10,000 years ago (see also Podisma, Ensatina, and Sceloporus grammicus).With data on many hybridizing groups, the correlation between their phylogeny and their geo- 134 BARTON & HEWITT graphic distributionmight, in principle, distinguish primaryfrom secondary contact (75, 245). However, the difficulties of inferringphylogenies make the statisticalpower of such an approachexceedingly weak (75). These argumentsonly concernthe age of present-dayzones; the differences involved may be much older. The extensive biochemical and chromosomal differencesfound acrossmany hybridzones (see below) andthe slow evolution of such changes (47, 134, 141) suggest that they may be very old indeed. For example, immunological (157), biochemical (237), and mitochondrialDNA (239) differences all suggest thatBombina bomina and B. variegata diverged 4-5 million years ago. Gene flow between the hybridizingtaxa may make this an underestimate(see below). ReproductiveIsolation and Introgression How freely can genes be exchangedbetween hybridizingtaxa? One of the most striking features of hybrid zones is the generally high electrophoretic differentiation associated with them. For 34 zones for which such data are available, an average of 14% of loci show clear allele frequency differences, suggesting that these zones greatly impede gene flow. Unfortunately, inferences cannot be made so easily. A moderatelystrong barrier (B 100U; cf Table 1) could preserve neutraldifferences for a long time (- 10,000 generations). However, since such differences accumulate very slowly, even in- termittentlyhybridizing populations could not diverge in the first place without a virtually complete barrier (136). The extensive divergence across hybrid zones perhapsindicates that enzyme differences are maintainedby selection, ratherthan that gene flow is low. Even if the enzyme differences are maintainedby selection, we can still use detailedtransects to estimategene flow. Enzyme dines arenever narrowerthan morphologicalclines, implying that enzymes are, at most, weakly selected. Any barriershould thereforeinduce a sharpstep, with a shape independentof the weak selection on the enzymes. Szymura's (237, and in preparation) detailed electrophoreticstudy of the hybrid zone between the fire-bellied and yellow-bellied toads (Bombina bombina and B. variegata), near Cracow in southernPoland, is one of the few cases good enough to given an estimate of barrierstrength. There are enough samples within the zone to tell us its width, and enough distant samples to show that allele frequencies do tail away to fixation (Figure 1; J. M. Szymuraand N. H. Barton, in preparation).Five loci are each fixed for different alleles on either side of the zone. All five show similargeographic patterns: a sharpstep, 6 km wide (95% limits 5.5-6.5 km), is flankedby much shallower tails (Figure la). This patterncould be produced by occasional long-distance migrants, ratherthan by the diffusion of genes throughthe zone; however, very few parentalor Fl genotypes are found in the tails. The steppedpattern is likely to be due to a barrier,whose strengthcan be ANALYSISOF HYBRIDZONES 135 estimatedfrom the dine shape. Averagingthe two sides, B equals 220 (38-440) km, or, given dispersal of au 900 m in a generation(see section below on Numberand Typesof GenesInvolved in HybridZones), B/au 240. This would delay the introgressionof a neutralallele for about32,000 generations.Howev- er, an allele with an advantageof 0.1% would only be delayed for about 1,500 generations. Bombina bombina and B. variegata are therefore conspecific, despite their extensive morphologicaland biochemical divergence. We have made similarestimates in the few othercases with sufficient data;the barrieris generally substantial,but certainly not absolute. Electrophoreticand chromosomaldines are often significantly asymmetric [Bombina, Mus musculus/domesticus,Ranidella, Uroderma, Caledia; see (173)]. Moreover, this asymmetryis often in the same directionat differentloci (e.g. Mus, Ranidella, Caledia). Individualalleles could be selected againston one side of the zone, but not the other;however, it is thenhard to accountfor the consistency across loci. More likely, gene flow is asymmetric;consistency is then to be expected. However, it is hard to make any inferences about the relativefitnesses of the two types, or aboutmovement of the hybridzone, from such asymmetry(see above). In some cases [e.g. Mus musculus/domesticusin Jutland (81); see (5)], though not in all [e.g. Bombina bombinalvariegata (239), Mus musculusl domesticusin SouthernGermany], mitochondrialDNA differences are shifted away from the set of coincident electrophoreticand morphological changes. Similardiscordance is also found in cases of sporadichybridization (5). Since mitochondrialgenes are less closely linked, on average, with nuclear genes than nuclear genes are with each other, and since the barrierto gene flow dependsexponentially on the harmonicmean recombination rate, this patternis not surprising(28).

Rare Alleles in Hybrid Zones

In most (19 out of 23) thoroughelectrophoretic surveys of hybrid zones, an increasedfrequency of rarealleles has been found (Tables 1, 2). It is hardto see how alleles which are usually at frequenciesof a few percent or less could be maintainedby balancingselection (148, 202). If, then, we assume thatthey are neutral or slightly deleterious, their increase could be caused by a higher mutationrate, by intragenicrecombination (175, 235), or by relaxed selection. The latterseems unlikely (thoughthe increaseof acrocentricsin the Sorex zone might be seen as an example; see below), but the first two are hard to distinguish.Increased mutation has received most attention(205, 269, 270), by analogy perhaps with the general evidence of breakdownin hybrid zones- morphological aberrations (Bombina, Pseudophryne, Warramaba viatica, Litoria, Enneacanthus), disruption of spermiogenesis (Caledia, Podisma, 136 BARTON& HEWITT

Chorthippusparallelus), and increased chromosomal mutation (Podisma, Caledia)-and with hybrid dysgenesis in Drosophila (76). The frequent excess of presumablydeleterious variants is strong evidence that most zones involve some hybrid unfitness. However, these aberrations need not necessarily contributemuch to the total selection acting in the zone. For example, the five-fold increase in rare alleles at two out of ten almost monomorphicloci in Podisma could be accountedfor by a mutationload of as little as 5 x 10-4 per locus (22). Nor is it clear whatevolutionary consequences might ensue from such phenomena. Although increased mutationmight pro- vide new advantageousalleles (269), the narrowregion in which these would be produced, and the availabilityof a great variety of recombinantsin this region make this relatively unlikely. The Number and Types of Genes Involved in Hybrid Zones The natureof the genetic differences across hybridzones and especially across tension zones is of considerableinterest, since these are likely to be similar to the differences that separate full species. The genetic basis of species divergence gives one of the few pieces of evidence that might bear on mechanisms of speciation (21, 54, 63, 159, 241). Perhapsthe most striking feature of hybrid zones is that zones ascertained throughone characterare usuallyfound to involve manyothers. Chromosomal, electrophoretic, morphological, behavioral, and mitochondrial DNA differences often coincide. This could be taken as evidence that these differences evolve together, in occasional "genetic revolutions" (160-162), or that coadaptationis so pervasivethat any initial change is amplifiedinto substantial divergence (55, 74). However, we think it more likely that the coincidence of charactersis simply due to their slow evolution, relative to the rate at which population restructuringbrings together independenttension zones. The genes thatcontribute to isolation are especially important.Hybrid zones can give better estimates of their numberthan are obtainablefrom laboratory crosses. While the latterare limited to a few generations,hybrid zones contain genotypesthat have been producedby recombinationover thousandsof generations. Two methodscan be used. First, the widthof the region of reducedhybrid viability, relative to the dispersalrate, gives the average selection maintaining each underlying line. Comparingthis with the total selection acting against hybridsgives a robustestimate of gene number[in Podisma, 150 (50-500) (25)]. Second, linkage disequilibriagive an estimate of the selection on the individualalleles observed, and any alleles associatedwith them. Disequilibria are expected to producea barrierto gene flow the strengthof which dependson the total selection and on the harmonicmean recombinationrate. If the latteris known, then the observed barrierstrength gives an estimate of the total selection. This can be comparedwith the selection estimatedfrom the disequilibria ANALYSISOF HYBRIDZONES 137 to give gene number [in Bombina, 500 (100-oo) (J. M. Szymura and N. H. Barton, in preparation)].These high estimates are consistentwith the generally high levels of divergenceacross hybrid zones andwith the usualpolygenic basis of species differences (21, 63, 159). They also supporttheoretical arguments thatreproductive isolation is more likely to arise in many weakly selected steps than by a few drastic substitutions(21, 257). White (259, 261, 262) has argued that chromosomal differences are of primaryimportance in causing speciation. However, chromosomaldifferences usually make up only one component of hybrid zones. More directly, they usually cause little nondisjunctionin heterozygotes[e.g. Podisma (16), Spalax (185), Caledia (211), Sorex (see section below on "Reinforcementand character displacement), Warramabaviatica (177, 178)]. Indeed, although the rarity of chromosomal polymorphism (141, 262) suggests the general importance of heterozygote disadvantage, there are many cases where other effects seem as important. Chromosome differences are directly associated with differences in DNA content and rDNA sequence in Podisma (258; J. Dallas, personal communication), and with differences in embryo weight in Caledia. "Karyotypicorthoselection" (260), where similarrearrangements are fixed on many chromosomes, is frequent (e.g. Caledia, Mus, Thomomys). Evidencefor Modification of Hybrid Zones Despite the popularityof the idea that selection may increase prematingisolation within hybridzones, there is remarkablylittle evidence for such reinforcement. We can find only 3 plausiblecases: Microhyla,Litoria, andPinus, out of 32 zones thatare knownto involve prematingisolation, and 12 in which explicit searches for reinforcementhave been made. Even where, as in these 3 examples, prematingbarriers are strongernear the zone, reinforcementmay not be the only explanation: Stam (232) has suggested that the divergence in flowering time between populationsof Agrostis adaptedto different levels of heavy metals could be caused by environmentaldifferences, ratherthan as an adaptationto reduce gene flow. Reinforcementcould be rarebecause it is hard to change the mating system, or because there is little genetic variationinside narrowhybrid zones (see section above on Modificationof HybridZones). The latteris perhapsmore likely, since thereis evidence that selection may increase isolation where two forms are sympatricover a large area (e.g. 70, 80, 122, 124). In some cases, isolation seems weaker within hybrid zones than elsewhere. For example, B. bombina and B. variegata taken from pure populationshave distinctcalls and show stronglyassortative mating preferences. In some places these two taxa remain fairly distinct in sympatry. However, within the hybrid zone at Cracow, electrophoretichaplotypes are combined randomly, with a heterozygote deficit of less than 1.2% (J. M. Szymura and N. H. Barton, in 138 BARTON & HEWITT preparation).This may be because loci affecting the mating system can only induce assortmentfor the small proportionof genes that are closely linked to them, or it may be that mate choice breaksdown when the populationconsists almost entirelyof highly recombinedhybrids. Hybridzones may be weakened in other ways. For example, several hybrid zones exist in the shrew Sorex araneus between metacentric karyotypes with different combinations of chromosome arms. Heterozygotes between these different metacentriccom- binationshave greatlyreduced fertility (J. B. Searle, personalcommunication). However, heterozygotes between any metacentric combination and an acrocentrickaryotype are much less sterile, with more or less normalmeiotic segregation.As a result, thereis a high frequencyof acrocentricchromosomes withinthe hybridzone (85, 209); these can be regardedas modifiersthat reduce selection againstchromosomal heterozygotes. In summary,hybrid zones may be modified in many ways; however, such modificationdoes not often seem to reduce hybridizationor to make hybrid zones unstable.

CONCLUSIONS

The characteristicspatial configuration of most hybridzones andthe wide range of genotypes found within them persuadeus that the great majorityare maintained in a stable balance between dispersal and selection. It is harder to distinguish whether parapatricallydistributed forms remain distinct because they are adaptedto differentenvironments, or because hybridsbetween them are less fit. However, both the direct evidence of hybrid unfitness and the indirect evidence of the close concordanceof different characterslead us to believe that the latter is more likely, and that most hybrid zones are in fact "tensionzones." Hybrid zones may remain in equilibriumfor long periods of time; perhaps the most striking feature to emerge from our survey is the extensive divergence between hybridizinggroups, which indicates that their divergence is ancient. Certainly,little evidence suggests thatthey are unstable toward the reinforcementof mating isolation. These narrow and persistent interfaces between distinct populations have suggested various theories of parapatricspeciation (e.g. 74, 83, 132, 259); much attentionhas thereforebeen focused on whether they were established throughprimary or secondarycontact. However, this questionis hardto answer and, in any case, may not tell us about the origin of genetic divergence. If hybridzones are indeed ancient, and in a stable equilibrium,all traces of their origin may have been lost. It seems more profitableto use hybridzones to investigate the natureof the genetic differencesthat separate divergent populations. We have shown thatthe pattern of genotype frequencies across a dine can give good estimates of parameterssuch as rates of gene flow, selection pressure,and numbersof loci, ANALYSISOF HYBRIDZONES 139 which would be hardto measurein any otherway. At present,only a handfulof studies have given enough geographic and genetic detail for such analysis (Table 1); we hope that over the next few years, this handful will be greatly increased.

ACKNOWLEDGMENTS

We thank R. Butlin, D. Currie, R. A. Nichols, and S. Rouhani for their thoughtfulcomments on the manuscript,and their help in preparingthe Figures and Tables; all those (too numerous to name) who gave us details of their unpublishedwork; and T. Tsang andS. Wardfor theirpatient typing. This work was supportedby grantsfrom the NERC and SERC to G. M. Hewitt, and from the SERC and the Nuffield Foundationto N. H. Barton.

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