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Population Structure of a Predatory Beetle: the Importance of Gene Flow for Intertrophic Level Interactions

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Population Structure of a Predatory Beetle: the Importance of Gene Flow for Intertrophic Level Interactions Heredity 72 (1994) 228—236 Received 7 July 1993 Genetical Society of Great Britain Population structure of a predatory beetle: the importance of gene flow for intertrophic level interactions MOSHE COLL*, LAURA GARCIA DE MENDOZA & GEORGE K. RODERICKt Department of Entomology, University of Maryland, College Park, MD 20742, U.S.A. Migrationand gene flow of natural enemies play an important role in the stability of predator—prey interactions and community organization in both natural and managed systems. Yet, relative to that of their herbivorous insect prey, the genetic structure of natural enemy populations has been little studied. We present evidence that populations of the predatory coccinellid beetle Coleomegilla maculata (Coleoptera: Coccinellidae), are not genetically subdivided and that levels of gene flow among these populations are extremely high. Furthermore, in the same geographical area, gene flow of C. maculata was significantly (one order of magnitude) greater than that of an abundant prey species, the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). The high mobility of this natural enemy relative to the insect herbivores on which it feeds may contribute to its effectiveness as a biological control agent in agricultural systems. Keywords:allozyme,biological control, electrophoresis, gene flow, metapopulation, natural enemies. Introduction Despite the recognized importance of mobility of natural enemies, little is known about their population Thegenetic structure of populations is a function of structure, especially the amount of gene flow their spatial arrangement and amount of gene flow (Roderick, 1992) and dispersal (CoIl, 1991) among among them. The extent of gene flow will determine field populations. This lack of information stands in not only the potential for populations to diverge gene- contrast to the studies of the genetic structure of herbi- tically but will also influence local population vorous insect populations in both natural (Slatkin, dynamics. For predatory species, these effects are also 1985a, 1987; McCauley & Eanes, 1987) and managed likely to be coupled with the dynamics and movement systems (Loxdale & den Hollander, 1989; Roderick & of their prey. The association between predator and Caldwell, 1992). prey is well illustrated, theoretically and experi- Many studies have examined the role gene flow mentally, by predators and parasitoids (collectively plays in the development of local adaptation in herbi- termed natural enemies) and the herbivorous insects vores, including the evolution of host races (Butlin, which they attack. For example, movement of natural 1990; Roderick, 1993) and the development of insecti- enemies may contribute to their aggregative response cide resistance in pest species (Comins, 1977; to sites harbouring varying numbers of prey (Murdoch Georghiou & Taylor, 1977; Taylor & Georghiou, et aL, 1985; Strong, 1988). Under some conditions, 1979; Tabashnik & Croft, 1982; Caprio & Tabashnik, such aggregative response by natural enemies may 1 992b). Selection pressure from pesticide application have, at least theoretically, stabilizing effects on popu- will also affect natural enemies (Rosenheim & Hoy, lations (Hassell, 1978; Hassell & May, 1988) or meta- 1986; Rosenheim & Tabashnik, 1991). In general, low populations (Taylor, 1991) of predators and prey. levels of gene flow may permit local adaptations such as the evolution of insecticide resistance (Caprio & Tabaslmik, 1 992b). If natural enemies are indeed more mobile than their hosts or prey (Murdoch et a!., 1985) *Correspondence. USDA, ARS, Insect Biocontrol Laboratory, then natural enemies may not develop insecticide BARC-East, Bldg. 402, Beltsville, MD 20705, U.S.A. resistance as rapidly as their herbivorous prey. In turn, tPresent address: Hawaiian Evolutionary Biology Program, University of Hawaii, 3050 Maile Way Gilmore 310, Honolulu, HI differences in susceptibility to insecticides between 96822, U.S.A. herbivores and natural enemies may facilitate pest out- 228 GENE FLOW IN A PREDATORY BEETLE 229 breaks and resurgence because of the removal of predators and parasites by pesticide applications. It is Methods unclear, however, how differences in gene flow between natural enemies and their herbivorous prey affect their susceptibility to insecticides. Biological material Two approaches are commonly used to estimate Thepredatory beetle C.maculatais native to North gene flow among populations: direct measures, such as America and is widely distributed east of the Rocky release—recapture, and indirect estimates based on pat- Mountains (Obrycki & Tauber, 1978). In both natural terns of genetic similarity among populations (Slatkin, and managed systems, larvae and adults are important 1985a, 1987). Although direct measures of dispersal natural enemies of aphids, insect eggs and soft-bodied represent actual observations, they may be biased by immatures (Smith, 1960; Atallah & Newsom, 1966; not reflecting rare gene flow events or non-random Warren & Tadic, 1967, and references therein). The contributions to subsequent generations (Ehrlich & predator is common in maize, alfalfa, cotton, potato, Raven, 1969; Endler, 1979; Slatkin, 1987). By tobacco, curcubits and cole crop systems (Ewert & contrast, indirect estimates of gene flow, based on FST Chiang, 1966; Richardson & DeLoach, 1973; Elsey, (Wright, 1951) or rare alleles (Slatkin & Barton, 1989), 1974; Wright & Laing, 1980; Marck & Smilowitz, reflect variations in allele distribution that were pro- 1982; Cosper etal., 1983; Groden etal., 1990; Coll & duced over long periods (Slatkin, 1987; McCauley, Bottrell, 1991; Hazzard et al., 1991). In potatoes, C. 1991). maculata can be a major natural enemy of the In this study, we first used allozyme electrophoresis Colorado potato beetle (Groden et al., 1990; Hazzard to examine the population structure of a predatory & Ferro, 1991; Hazzard et at., 1991). beetle, Coleomegilla maculata De Geer (Coleoptera: Six populations of overwintering adult C. maculata Coccinellidae). Then, we tested the hypothesis that were sampled in Maryland, U.S.A., between 31 March level of gene flow among populations of this predator is and 10 April 1992 (Fig. 1). The sampling sites were in greater than that among populations of one of its sym- the following counties: Washington (39°30'55"N; patric abundant prey species, the Colorado potato 77°44'50"W), Frederick (39°16'05"N; 77°28'05"W), beetle, Leptinotarsa decemlineata Say (Coleoptera: Montgomery (39°1 7 '30 "N; 77°1 2'25 "W), Howard Chrysomelidae). (39°12'45"N; 76°56'lO"W), Prince George I I I 0 25 50 75 100 1cm Fig. ICollectionsites of six Coleomegilla maculata overwintering aggregations in Maryland, U.S.A. 230 M.COLLETAL. (39°00'40"N; 76°49'55"W) and Anne Arrundel these enzyme systems were adopted from Hebert & (38°55 '50 "N; 76°3 7 '45 "W). The approximate distance Beaton (1989). Electromorphs were labelled alpha- between the westernmost and the easternmost popula- betically with 'A' as the fastest running electromorph. tions was 116 km. The beetles were collected from overwintering aggregations at the base of prominent Genetic trees at the edge of maize fields. Since C. maculata analysis does not exhibit a long distance migratory behaviour to Thefixation index, FST is a measure of genetic dif- overwintering sites (Hagen, 1962), all beetles collected ferentiation among populations and can range between from the same aggregation are considered to belong to 0 (no genetic differentiation) and 1 (complete dif- the same population or random breeding unit. The ferentiation) (Wright, 1951). It has several equivalent beetles were maintained in the laboratory (25 3°C interpretations. FST can be expressed as the absence of 15:9 L : D) until they were no longer in diapause heterozygotes in subpopulations relative to what is (determined by flight and feeding behaviours) and after expected in the total population (i.e. FST= (HT HS)/HT, any parasitoids (Dinocampus (=Perilitus)coccinellae where H is the average heterozygosity of subpopul- (Hymenoptera: Braconidae)) had emerged (about 25 ations and HT is the predicted total heterozygosity). FST April). The beetles were frozen at —80°Cuntil pre- also represents the standardized variance in allele fre- paration for electrophoresis. quencies among local populations (Weir, 1990). While these formulations of FST are for one locus and one allele, similar statistics can be estimated for two alleles Electrophoresis at one locus (Wright, 1951) and for more alleles at Cellulose-acetategels (Helena Laboratories Inc.) were many loci (as GST; Nei, 1973, 1977; Birky eta!., 1989). used for electrophoresis (Richardson et al., 1986; An alternative to FST is the statistic of coancestry, 0, Hebert & Beaton, 1989). Before electrophoresis, which represents the correlation of genes of different beetles were homogenized individually in 50 4u1 of dis- individuals in the same populations (Weir & Cocker- tilled water and centrifuged for 5 mm at 4°C. Resolving ham, 1984; Weir, 1990). gels were maintained at 4°C during electrophoresis. A For neutral alleles, FST, GST or 0, can be used to preliminary survey of 17 enzyme systems revealed nine estimate the number of migrants exchanged by popula- polymorphic resolvable loci. The following seven tions per generation (gene flow) (FST =1/(4Nem+ 1), enzyme systems encoded by nine presumptive loci where Ne is the effective local population size and m is were scored in all six populations: fumarate hydratase the average
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