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Systems in the Australian Sheep Blowfly Lucilia Cuprina

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Systems in the Australian Sheep Blowfly Lucilia Cuprina HeredityG7 (1991) 365—371 Received 2 February 7991 OThe Genetical Society of Great Britain Male crossing over and genetic sexing systems in the Australian sheep blowfly Lucilia cuprina GEOFFREY G. FOSTER, GAVE L. WELLER & GEOFFREY M. CLARKE CSIRO Division of Entomology. GPO Box 1700, Canberra ACT 2601, Australia Field-femalekilling (FK) systems based on deleterious mutations arid Y-autosome translocations are being evaluated for genetic control of the Australian sheep blowfly, Lad/ia cuprina. Experience during field trials has shown that mass-reared colonies of FK strains are subject to genetic deterioration, caused mainly by genetic recombination in males. A previous study found higher male recombination frequencies in two Y-linked translocation strains than in chromosomally normal males. However, the results of the present study indicate that breakage of the Y chromosome is neither sufficient nor necessary for increased levels of male recombination. The fre- quency of male recombination appears to be unrelated to the presence of specific chromosome rearrangements. Keywords:genetic control,genetic sexing, Lad/ia cuprina, male recombination. FTC-strain females are homozygous for one or more Introduction eye-pigment mutations and have white eyes. They can Geneticsexing systems facilitate separation or killing of survive in cages, but they are functionally blind, rarely mass-reared insects according to sex. This is most surviving long in the field; in other words the eye- frequently accomplished by artificially linking appro- colour mutations are recessive lethals under field con- priate mutations with sex using rearrangements ditions (Whitten ci at, 1977). between sex-determining chromosomes and other FK-strain males carry the eye-colour mutations on a chromosomes, although other sex-determining mech- single set of normal autosomes, and the wild-type anisms can be exploited (reviewed by Whitten & Foster, alleles on the translocation. They have normal eye 1975). Insects with Y-mediated sex determination, pigmentation and vision, and are competitive in the such as most higher Diptera (Boyes, 1967; Ullerich, field, transmitting the translocation to their sons and 1963) are especially amenable to genetic sexing. the mutations to their daughters. Genetic sexing may assist in rearing economically When the daughter of a released FK male, hetero- important insects such as silkworms (Tazima, 1964), or zygous for the mutations, is mated by a released male, a in genetic pest control strategies involving release of proportion (half or more, depending on the number of sterilized or genetically altered males. mutations) of her daughters is homozygous and thus In Australia a genetic sexing system which operates unable to survive to reproductive maturity (Whitten a in the field is central to proposed large-scale control at,1977; seefig. 1 of Foster etal., 1985 or 1988). programmes against the blowfly Lad/ia cuprina, a Matings of wild females by released FK-strain males major myiasis pest of the Australian sheep industry lead to reduced population fertility from the semi- (Foster, 1989; Foster et at, 1985, 1988; Whitten, sterility of the translocation and, with sustained 1979; Whitten a at, 1977). This field-female killing releases, a high frequency of homozygosis for the (FTC) system combines recessive conditional-lethal mutations in non-translocation zygotes of field origin mutations with a translocation involving the Y chromo- (Foster ci at, 1985, 1988; Whitten, 1979; Whitten ci some and two autosomes. a/., 1977). Semisterility and homozygosis combine to give genetic death rates approaching 94 per cent with Correspondence: Dr G. 0. Foster, CS1IRO Division of Entomology, presently available FTC strains of L. cuprina. This GPO Box 1700, Canberra ACT 2601, Australia. system has successfully suppressed sheep blowfly 365 366 G. 0. FOSTER, ETAL. populations in two field trials conducted in 1984—86 1984). In field trials this has contributed to serious (R. J. Mahon, T. L. Woodburn and G. C. Foster, genetic deterioration of release strains (Foster et a!., unpublished observations). 1985; Hooper eta!., 1987). For long-term pest suppression campaigns FK In a previous study, L. cuprina males carrying either systems are likely to be more cost-effective than the of two related 'V-linked translocations showed cross- sterile-insect technique (Sn), since at low release rates over frequencies several times higher than in chromo- FK males can cause higher genetic death rates in somally normal males (Foster et at, 1980a). Rdssler density-influenced populations than sterile males (1982a, b) reported male recombination in Ceratitis (Foster eta!., 1988). capitata, but his data suggested little difference Geneticsexing requires tight linkage of particular between translocation and normal strains. The present autosomal mutations to sex. In most higher Diptera, the study was aimed at discovering whether or not the frequency of crossing over in males is usually several apparently increased frequency of male recombination orders of magnitude lower than in females (Foster et in Y-linked translocation strains of L. cuprina (Foster et a!., 1980a; Milani, 1975; Rbssler, 1982a; Rdssler & a!., i980a) is caused by rearrangement of the Y or Rosenthal, 1990). It has been tacitly assumed that in other chromosomes. this group of insects, the difference in crossover frequency between the sexes would give sufficiently Materials and methods tight linkage in genetic sexing systems using Y-linked translocations (Foster et at, 1978; McDonald, 1971; Mutations and strains Robinson & Van Fleemert, 1982; Wagoner eta!., 1974; Whitten, 1969, 1979; Whitten eta!., 1977; Whitten & The names and symbols of mutations mentioned in the Foster, 1975). present report are as follows: chromosome 3: white However, genetic sexing systems are vulnerable to eyes (w), rusty body (ru), featherless aristae (ar), low levels of make recombination. Such recombination yellowish eyes (yw); chromosome 4: radial vein gaps may separate one or more of the mutations from the (ra), short bristles (sh), singed vibrissae (sv), golden male-determining region of the Y chromosome. If the body (gl); chromosome 5: Fused veins (Fv), topaz eyes products of such recombination enjoy a selective (to), stubby bristles (sby). Female linkage data for these advantage in rearing colonies, linkage of the critical mutations are contained in Foster et a!. (1981)(also see mutation to sex can rapidly disappear (Busch-Petersen, Table 1). Complete descriptions, origins and other 1989; Foster et at, 1980a; Hooper el at, 1987; Saul, information are given by Maddern ci at (1986). Table I Effects of translocations on crossing over on chromosome 3 in both sexes Autosomal Number ofTotal CrossoverFrequencies Genotype breakpoints* matingst progenytie— or or—yw Females Nontrans, Fv 12 2,430 0.3305 0.0790 Nontrans, S/r 12 1,994 0.3235 0.0S52' T(3;5)411,Fv33B;74A 12 1,988 0.2862 0.0734b T(4;5)357, Sb49A; 70C/71A 12 2,079 0,3002 0.0991' T(3;4)230 34A;SOA 12 2,324 0.2229 0.1011' Males Nontrans, Fv 33 5,637 0.0016 0.0000 Nontrans, Sb 28 5,160 0.0004 0.0000 T(3;5)411, Fv3313; 74A 42 5,628 0.0121' 0.0000 T(4;5)357, SI, 49A; 70C/71A 33 3,205 0,0047b 0.0000 T(3;4',1230 34A; 50A 38 5,291 0.0000 0.0000 *Numerals and letters indicate standard polytene map regions (Foster flat, 1980k,): chromosome 3, regions 21A—40C; chromosome 4, regions 41A—60D; chromosome 5, regions 6 lA—SOD; chromosome 6, regions 81A—100B; Slash (/) indicates breakpoint at junction of regions. tAll tests from single-pair matings. Homogeneity tests; b, c =crossoverfrequency heterogeneous between pairs, PC 0.01, 0.001, respectively. MALE RECOMBINATION AND GENETIC SEXING IN L. CUPRINA 367 The 15 translocations used in the present study were Results induced, over a period of several years, by irradiating mature sperm (5-day-old males) (2800 rads gamma Dataon the effects of three translocations on crossing rays from a 60Co or a 137Cs source) and using a number over in chromosome-3 in both sexes are summarized in of crossing schemes to detect linkage of genetic Table 1. in females, crossover frequencies were markers on heterologous linkage groups (e.g. Foster & generally similar in translocation and non-translocation Whitten, 1974). The translocations T(4;5)357,Sh crosses. With the possible exception of T('3;4,)230, (Foster.1982),T(3;5)411,Fv, T(Y5)529,Fv and crossover frequencies for the ru to ar and ar to yw T(3;5)530,Fv were induced in laboratory strains con- regions were consistent with earlier data for these taining the dominant mutations S/i or Fv, respectively. intervals (Foster et at, 1 981). The others were induced in a succession of wild type In the reciprocal crosses, the results were very strains derived from mass field collections near different (Table 1). First, crossover frequencies were Canberra in the 1 970s (T(3;4)230 and T('3;4)257) and considerably lower in males than in females. Secondly, (all other translocations) near Canberra in 1983 and in two of the translocation crosses male crossover 1985, and on Flinders Island, Bass Strait in 1987. frequencies were an order of magnitude higher than in Thus genetic background was not uniform in these the non-translocation crosses, while in the third trans- studies. location cross no crossovers were recovered. These Translocation break points were determined using results cannot be explained as localized effects of par- trichogen-cell polytene chromosomes prepared as ticular translocaticm breakpoints, since one of the shown by Bedo (1982) and classified according to the rearrangements did not involve chromosome 3, and system of Foster et al. (1980b) in which the standard the two which did involve this chromosome had similar polytene chromosome map is divided into 100 regions chromosome-3 breakpoints (regions 33B and 34A, (20 regions per autosome). respectively) (Table 1). Male recombination was examined in a further series of crosses using various combinations of trans- Recombinationassay procedure locations and genetic markers.
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