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Of Warning Colour Dines Heredity 56 (1986) 191-202 The Genetical Society of Great Britain Received 12 July 1985 Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning colour dines James MaIIet* Department of Zoology, University of Texas, Austin, Tx. 78712, U.S.A. Heliconius erato and H. melpomene are warningly coloured tropical butterflies that show mimetic covariation throughout the neotropics. Central American, West Colombian, and North Colombian colour pattern races of both species meet and form hybrid zones in Panama. These hybrid zones were sampled along a transect. The major colour pattern changes are determined by three alleles at a single locus in each species. There is no evidence for hybrid breakdown or mating incompatibility between any of the phenotypes in Panama, and local genotypic frequencies are not significantly different from Hardy-Weinberg expectation. I simulated a single-locus, two-allele warning colour hybrid zone (dine) with dominance. Predator selection on warning colour patterns was assumed to be frequency-dependent, so that, at any point in the dine, a rare phenotype has lower fitness than a common phenotype. Simulation shows that such a dine rapidly reaches a stable slope. Since the model does not depend on selection caused by the abiotic environment, the dine is positionally unstable. Even if the two phenotypes are equally fit "dominance drive" tends to increase the area in which the dominant allele is present. Differences in fitness of the phenotypes and density gradients can also cause dine movement. Hybrid zone movement might either be rapid enough to obliterate patterns that were formed in Pleistocene refugia, or so slow as to make secondary contact a requirement for the existence of hybrid zones. A third possibility is that local variations in population density will normally prevent hybrid zone movement, even if this is potentially rapid. Better estimates of dispersal and selection are needed to resolve this issue. INTRODUCTION Species of the butterfly genus Heliconius often have large numbers of colour-pattern races with Manygroups of closely related taxa are distributed parapatric distributions, connected by hybrid in patchwork patterns, with their ranges abutting. zones (Brown and Mielke, 1972; Brown eta!., 1974; These "parapatric" forms are often separated by reviewed by Brown, 1976; 1982; Turner, 1982). The narrow zones of hybridisation. For the purposes standard explanation has been that this raciation of this paper, I define hybridisation as the process occurred in allopatric Neotropical refugia during of obtaining offspring (hybrids) in natural or Pleistocene dry periods (Turner, 1965; Brown et artificial crosses between genetically distinct strains, a!., 1974; Brown, 1982; Turner, 1982). Recently, a and hybrid zone as a narrow zone of genetic change number of authors have suggested that parapatric (where natural hybrids occur) between the ranges of differentiation is equally consistent with the avail- two parapatric, genetically distinct forms. These able evidence from Heliconius (Endler, 1977; 1982; definitions are useful because they are based on White, 1978; Benson, 1982). Much of this work the phenomena themselves rather than on the has centred on Heliconius erato and H. melpomene, unknown causes of the phenomena. I use neither which are common, well collected, and have very history (Mayr, 1970: 69), nor fitness or stability well-known biology (Emsley, 1964; Brown, 1981; (e.g., Endler, 1977; Barton, 1979; Barton and Turner, 1981). These two species have phenomenal Hewitt, 1981) to define hybridisation and hybrid parallel geographic variation in colour pattern, zones. which provides one of the best pieces of evidence *Present address: GaltonLaboratory, Department of Genetics for the existence of mimicry (see Turner, 1982). and Biometry, University College of London, 4 Stephenson Major colour pattern differences between races of Way, London NWI 2HE. both species are usually controlled by a few Men- 192 J. MALLET delian factors (Turner, 1982; Sheppard et a!., gotes (shown schematically in fig. 1). In H. mel- 1985). Both species are distasteful to birds, and pomene, the West Colombian yellow bar (on under- their colour patterns are almost certainly selected side only) is dominant to the Central American for warning coloration and Müllerian mimicry bar (on upper and underside), and recessive to (Brower et a!., 1963; Brower and Brower, 1964; lack of bar, but the inheritance of the West Colom- Benson, 1972). Widths of hybrid zones in H. erato bian pattern is not known for H. erato. and H. melpomene have been reported to be 10- The purposes of this study were to obtain data 200km wide (Benson, 1982; Brown and Mielke, on the shapes, widths, and genetics of hybrid zones 1972; Turner, 197 Ia), but detailed transects have of H. erato and H. melpomene in Panama, and to not been made, and the genetics of the zones is investigate the fitnesses of hybrids and the stability often not known. The lack of detailed work in of interactions in the zones. Heliconius hybrid zones makes it hard to guess how they originated and how they are maintained. MATERIALSAND METHODS Three races of H. erato meet in Panama (See fig. 1): (1) a "Central American" race which has Thestudy was carried out in three parts: (1) a red forewing band and a yellow hindwing bar phenotypes of H. erato from the hybrid zone were (distributed from Northern Mexico south to intercrossed to determine the inheritance of colour Eastern Panama); (2) a "North Colombian" race pattern; (2) samples of H. erato and H. melpomene which is similar to the Central American race but were taken along a transect through the hybrid which lacks the yellow bar (distributed from the zones; and (3) a simulation model of a hybrid zone Guianas east through Venezuela to North-Central was constructed and used to analyse the genetic Colombia); and (3) a "West Colombian" race data. which is also similar to the Central American race, except that its yellow bar is expressed on the under- Laboratory crosses of H. erato. Since the known surface only (distributed in Colombia west of the genetics of hybridisation had been deduced from Western Cordillera of the Andes). For simplicity, allopatric crosses (e.g., Mexico x Trinidad), and the currently accepted scientific names of the races since some of the genetics were not known for H. are not used here, but are given in table 1. There erato, I performed crosses of H. era to using hybrid are also minor colour pattern differences between zone stock. Adults were kept in outdoor insectaries the races (see Results). The distributions of these in Panama City, using techniques given by Turner races are shown in fig. 2. Heliconius melponiene (1974). The eggs were separated individually and has an overall pattern of racial variation similar their hatch rate recorded. Larvae were reared to to that of H. erato (see fig. 1 for phenotypes), maturity, and the adults were scored for the follow- which is almost certainly due to Müllerian mimicry ing: sex; yellow hindwing bar (presence, shadow (Brown et a!., 1974). The minor color pattern ele- or absence); yellow bar type if present (Central ments in H. melpomene also track their analogues American or West Colombian); upperside blue in H. erato. The genetics of some of the colour iridescence (scale 0—1); markedness of distal white pattern differences between these races has been fringes (scale 0—1); and size (forewing length). studied by Sheppard et al. (1985) and Mallet et a!. Wild-mated female parents were collected in (unpubl.). In both species the presence of the hind- Garachiné for broods PA1-PA2; and in TortI for wing yellow bar is determined by a single allele broods PA3-PA6 (table 2). They were allowed to which is almost completely recessive to absence of deposit eggs until their first progeny began to yellow, although a shadow can be seen in the black enclose from the pupa. Females of these progeny, pigment of the underside bar region of heterozy- and females reared from field-collected larvae were then mated to field-collected males chosen to test Table1 Trinomial nomenclature of Heliconius races in hypotheses of colour pattern inheritance (table 2: Panama hybrid zones broods PA7-PA12). The following parents in table 2 were reared from earlier broods: the female Heliconius Heliconius Name of race used erato melpomene parent of PA8 is from PA2; female parents of PAl 0, inthis paper subspecies subspecies PAll and PA12 are from brood PA!. The female parent of PA7 was reared from a larva collected Central American petiverana rosina in Puerto Obaldia, that of PA9 from a larva collec- West Colombian venus vulcanus North Colombian ted in PiriatI. A single male from Torti fathered hydara melpomene broods PA8, PA9, PAll, and PA12, and the male Source: Brown (1976; 1979) parents of PA7 and PAlO were also from TortI. HELICONIUS HYBRID ZONES 193 under upper North Colombian or or'T'Ywc Yyco Ca __l Heterozygote Central American Me/porn ene Era to Figure1 Phenotypes and genotypes of Heliconius melpomene and H. erato found in the Panama hybrid zone. The phenotypes correspond to races as follows: A, North Colombian race. B, Heterozygote between West Colombian or Central American, and North Colombian races. C, West Colombian race. D, Central American race. Genotypes shown conform to the results obtained in crosses. 194 J. MALLET CARIBBEAN SEA Transect 7 9 Race / PACIFIC OCEAN 0 km 00 W. Colombian Race Figure 2 Distribution of colour pattern races of H. eratoinPanama, showing sample sites and transect. See table 4 for exact locations and names of sample sites. Heliconius females are almost monandrous (Boggs, tional samples from sites away from the transect 1979), and show sperm precedence for their last were also collected. Precise collecting locality data mating (L. Gilbert, pers. comm.), so it was possible is given in table 4.
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