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Analysis of Hybrid Zones Author(S): N 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 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology and Systematics. http://www.jstor.org Ann. Rev. Ecol. Syst. 1985. 16:113-48 Copyright? 1985 by Annual Reviews Inc. All rights reserved 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, move- ment, 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 genotyp- ic 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,
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