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Genetic Differentiation and Natural Hybridization Between Two Morphological Forms of the Common Woodlouse, Oniscus Asellus Linnaeus 1758

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Genetic Differentiation and Natural Hybridization Between Two Morphological Forms of the Common Woodlouse, Oniscus Asellus Linnaeus 1758 Heredity 82 (1999) 462±469 Received 16 September 1998, accepted 13 January 1999 Genetic differentiation and natural hybridization between two morphological forms of the common woodlouse, Oniscus asellus Linnaeus 1758 D. T. BILTON* , D. GOODEà & J. MALLET§à Department of Biological Sciences and Plymouth Environmental Research Centre, University of Plymouth, Drake Circus, Plymouth PL4 8AA, U.K., àNatural History Museum, Cromwell Road, London SW7 5BD, U.K. and §Galton Laboratory, Department of Biology, University College London, 4 Stephenson Way, London NW1 2HE, U.K. The common woodlouse Oniscus asellus can be divided into two forms on the basis of morphology, particularly male accessory genitalia. Where these taxa meet, morphological intermediates are found, and the forms were therefore described as subspecies; O. a. asellus and O. a. occidentalis. In this study allozyme loci are used to test the hypothesis that intermediate forms result from hybridization, and to study the nature of hybridization. Thirteen enzyme loci were scored across ®ve English sites representative of each subspecies and intermediates. Ten loci showed strong frequency dierences between asellus and occidentalis populations, although no loci showed completely ®xed dierences. These data con®rm that asellus and occidentalis represent genetically distinct taxa, and that intermediate populations are of hybrid origin. There is apparently substantial population substruc- turing in the contact zone, as indicated by de®cits of heterozygotes (FIS) and sporadic gametic (i.e. linkage) disequilibria. Population structure in the Oniscus hybrid zone appears to be analogous to that seen in plant hybrid swarms rather than the narrow hybrid zones observed in many animal taxa. Values of Nei's genetic distance between the subspecies range from 0.65 to 0.70; these are much higher than between typical conspeci®c taxa and are indicative of ancient genetic divergence. However, because asellus and occidentalis do not remain distinct in areas of overlap, it is simplest to regard these taxa as members of the same species. Keywords: allozymes, hybrid zone, linkage disequilibrium, Oniscus, subspecies. Introduction habitats. Bilton (1994) suggested that the numerous populations with intermediate morphology arose via The woodlouse Oniscus asellus Linnaeus is one of the hybridization between the two subspeci®c taxa. This most widespread and abundant terrestrial arthropods paper presents the results of an allozyme study of ®ve in Western Europe. Bilton (1994) demonstrated that populations of Oniscus asellus s. lat. to test the the species could be divided into two distinct subspe- hypothesis that hybridization explains the intermediate cies: Oniscus asellus asellus Linnaeus and O. asellus morphologies found, and to study the nature of the occidentalis Bilton. The two taxa are ecologically and hybridization. We provide genetic evidence of strong biogeographically distinct as well as diering in mor- divergence between the taxa and discuss the status of phology. True asellus is widespread, particularly in these forms. synanthropic (human-in¯uenced) sites. On the other hand, occidentalis is recorded only from sites in the Materials and methods south-west of the British Isles and western France (Bilton, 1994, 1997). Intermediate populations occur Site selection and specimen collection throughout the range of occidentalis, and also further east, where they are increasingly con®ned to wet Oniscus specimens were collected from three sites in Devon (Wistman's Wood [ancient Quercus petraea wood- land; occidentalis], Lydford Gorge [managed mixed *Correspondence. E-mail: [email protected] woodland; intermediates] and Braunton [village garden; 462 Ó 1999 The Genetical Society of Great Britain. WOODLOUSE HYBRID ZONE 463 intermediates]) together with sites in Northumberland of loci polymorphic (95 and 99% criteria) and mean (Riding Woods [seminatural Quercus robur wood; as- heterozygosity. Population structure and deviations ellus]) and London (Highbury [urban garden; asellus]). from Hardy±Weinberg equilibrium were assessed using At each locality Oniscus specimens were collected by F-statistics (Wright, 1965, 1978). hand searching in humid shelter sites such as beneath To display the genotypic structure within the hybrid moss and bark on rotting logs. Only males were selected zone, a `hybrid index' was constructed based on allelic because female occidentalis and intermediate morphs are dierentiation between the two taxa. Alleles at each of not reliably separable from asellus (Bilton, 1994). Wood- the 10 dierentiated loci were classed as typical of either lice were brought alive to the laboratory, where they were asellus or occidentalis. The hybrid index value of an scored as asellus, occidentalis or intermediates on the basis individual represents the proportion of asellus alleles of male genitalia, before being transferred directly to a that it carries, and varies between 0 and 1. )70°C freezer for storage prior to allozyme studies. To assess population structure and gene ¯ow between the two taxa further, pairwise linkage disequilibria Allozyme electrophoresis (gametic correlations) were estimated for each popula- tion between each of the 10 dierentiated loci. Because For allozyme studies the head and pereon (leg-bearing we were interested in gene ¯ow between taxa, we lumped segments) of each individual were removed, and the alleles at each locus if they belonged to the same taxon. pleon (hind body) stored in ethanol for further study of Thus each locus was treated as if it had only two alleles: the accessory genitalia. Each pereon was homogenized O (occidentalis) and A (asellus). With 10 loci, this in 100 lL of grinding buer (0.1 M Tris/HCl pH 8.0; procedure also reduces the number of pairwise disequi- ®ve drops of b-mercaptoethanol/100 mL). The homog- libria to be estimated to 45 per site. Maximum enate was then centrifuged for 5 min at 10 000 g in a likelihood pairwise linkage disequilibria were calculated microcentrifuge and stored on ice. and their signi®cance tested following Hill (1974). We estimated the correlation coecient Rij to within an Electrophoresis and enzyme staining accuracy of 0.01 for each pair of loci i and j. The correlation coecient is calculated because it varies A total of 23 enzyme systems were initially screened. Of between 0 and 1, allowing a comparison of disequilibria these, 12 (aconitase, adenosine deaminase, adenylate between loci of dierent frequencies. The correlation kinase, esterase, fumarase, glucose-3-phosphate dehy- coecient is a standardization of the disequilibrium drogenase, glucose-6-phosphate dehydrogenase, a-glu- coecient, D , as follows: cose phosphate dehydrogenase, glutathione reductase, ij hexokinase, isocitrate dehydrogenase and nucleoside phosphorylase) showed no activity or were unscorable, Dij Rij p : leaving 11 enzyme systems with a total of 13 scorable pi 1 pipj 1 pj loci (acid phosphatase, Acp; enolase, Eno; glutamic- oxaloacetic transaminase, Got-1, Got-2; glucose-6-phos- The correlation coecient has been criticized as a phate isomerase, Gpi; malate dehydrogenase, Mdh; measure of linkage disequilibrium on the grounds that malic enzyme, Me; mannose-6-phosphate isomerase, it is dependent on the allele frequencies p and p Mpi; peptidase (leucine glycine glycine), Lgg-1, Lgg-2; i j (Hedrick, 1987). However, the alternative standardiza- peptidase (phenylalanine proline) Pp; phosphoglucomu- tion recommended by Hedrick (Lewontin's D *) has its tase, Pgm; and sorbitol dehydrogenase, Sdh). The ij own problems: although its limits are not frequency- running conditions on cellulose acetate gels were: Acp, dependent, its value is frequency-dependent; D * is also Eno, Got-1, Got-2 and Mdh, phosphate buer, 20 min at ij statistically intractable because it is a discontinuous 200 V; Pp, Tris-glycine, 15 min at 200 V; all other function (Lewontin, 1988). There is no easy solution to enzymes, Tris-glycine, 20 min at 200 V. Buers were as this problem of standardization, which is useful to follows: Phosphate buer, 20 mM NaH PO , 6 mM 2 4 compare disequilibria across loci which dier in p and Na HPO , pH 6.3; Tris-glycine, 20 mM Tris base, i 2 4 p . We here adopt the correlation coecient which is at 200 mM glycine, pH 8.0. Enzyme staining followed j least familiar from other statistical problems. Hill's Easteal & Boussy (1987), Emelianov et al. (1995) and likelihood method for estimating the within-gamete Richardson et al. (1986). disequilibrium, Dij, implicitly makes the assumption that the between-gamete disequilibrium, D , is zero Data analysis i/j (Weir, 1990). This assumption seems reasonable pro- The following were calculated for each of the ®ve vided that FIS 0 (FIS is essentially a within-locus localities: mean number of alleles per locus, percentage between-gamete disequilibrium). Unfortunately, we ®nd Ó The Genetical Society of Great Britain, Heredity, 82, 462±469. 464 D. T. BILTON ET AL. here that FIS is frequently nonzero, although the reasons which clearly characterizes the morphologically inter- for this may be in some cases more to do with scoring mediate Braunton and Lydford populations as genet- diculties or possible hemizygosity of sex-linked loci ically intermediate. These also had allele frequencies at than true absence of heterozygotes. Because the gametic diagnostic loci intermediate between those of Wist- arrangements of double heterozygotes cannot be detect- man's Wood (occidentalis) or London/Northumberland ed from allozyme data, our
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