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. 2014 Oct 7;281(1792):20141372.
doi: 10.1098/rspb.2014.1372.

Genetic elimination of field-cage populations of Mediterranean fruit flies

Philip T Leftwich  1 , Martha Koukidou  2 , Polychronis Rempoulakis  3 , Hong-Fei Gong  2 , Antigoni Zacharopoulou  4 , Guoliang Fu  2 , Tracey Chapman  5 , Aris Economopoulos  6 , John Vontas  6 , Luke Alphey  7
Affiliations

Genetic elimination of field-cage populations of Mediterranean fruit flies

Philip T Leftwich et al. Proc Biol Sci. .

Abstract

The Mediterranean fruit fly (medfly, Ceratitis capitata Wiedemann) is a pest of over 300 fruits, vegetables and nuts. The sterile insect technique (SIT) is a control measure used to reduce the reproductive potential of populations through the mass release of sterilized male insects that mate with wild females. However, SIT flies can display poor field performance, due to the effects of mass-rearing and of the irradiation process used for sterilization. The development of female-lethal RIDL (release of insects carrying a dominant lethal) strains for medfly can overcome many of the problems of SIT associated with irradiation. Here, we present life-history characterizations for two medfly RIDL strains, OX3864A and OX3647Q. Our results show (i) full functionality of RIDL, (ii) equivalency of RIDL and wild-type strains for life-history characteristics, and (iii) a high level of sexual competitiveness against both wild-type and wild-derived males. We also present the first proof-of-principle experiment on the use of RIDL to eliminate medfly populations. Weekly releases of OX3864A males into stable populations of wild-type medfly caused a successive decline in numbers, leading to eradication. The results show that genetic control can provide an effective alternative to SIT for the control of pest insects.

Keywords: medfly; release of insects carrying a dominant lethal; sterile insect technique.

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Figures

Figure 1.
Figure 1.
Life-history traits of fsRIDL strain flies, visualization of RIDL transformation marker and RIDL construct details. (a) Key elements of transgenic constructs: OX3864 and OX3647 use a tetO–tTA positive feedback system to give tetracycline-repressible lethality [26,31], rendered female-specific by addition of two sex-specific alternative splicing introns from two different tephritid species (to avoid repetitive genetic elements and the risk of recombination): Bactrocera zonata, BzTra (GenBank accession: BankIt1696174 BzTra KJ397268), and Ceratitis capitata, CcTra [28]. Only females produce splice variants encoding functional tTA protein. OX3864 and OX3647 differ in the promoter used for DsRed2. OX3864 used HR5 IE1, whereas OX3647 used polyubiquitin. (b) DsRed2 fluorescence renders the RIDL males (middle, OX3647Q; right, OX3864A) easily and reliably distinguishable from wt (left). (c) Same adults as in panel (b), under white light. (d) Survival under stress test conditions, i.e. without food or water post-eclosion. Adult male and female survival data are combined (n = 180). (e) Survival under non-stressed conditions of ad libitum food and water (n = 180), OX3647Q showed significantly reduced survival relative to wt. (f) Female lifetime egg productivity: average production from three cages of 30 females over three weeks. Wt lines produced more eggs than the other three lines; OX3864A produced more eggs than tsl and OX3647Q. (g) Individual female lifetime fecundity: no difference between the strains in the average number of eggs laid per female. (h) Hatching rates of eggs laid by the females in panel (g). tsl and OX3647Q had reduced egg hatch rates relative to wt, OX3864A did not differ from wt. All values are mean (±s.e.) unless otherwise stated.
Figure 2.
Figure 2.
Changing medfly population dynamics through introduction of OX3864A males into large cages of stable wild-type medfly populations. (a) Average daily egg production for each week in treatment and control cages. Weeks 0–8 constituted the population stabilization period (230 pupae added each week). Introductions of 1700 OX3864A pupae into each treatment cage commenced from week 8 onwards, in addition pupal return to each treatment cage was made proportional to the control cages. Six weeks after OX3864A male introductions, there was a clear reduction in egg production in the treatment cages compared with the control cages, continuing until eventual extinction of the wild-type population in both treatment cages (as assessed by two weeks of no egg production) by week 22 (14 weeks post initial RIDL release). The dotted line denotes the average weekly daytime temperature (Celsius) taken from daily midday temperature readings. (b) Numbers of females in treatment and control cages. (c) Proportion of progeny returned to each of the treatment cages from the oviposition traps displaying the DsRed2 fluorescent phenotype. Percentage of returning pupae carrying a copy of the OX3864A transgene reached 100% in both treatment cages by week 17 (11 weeks post-RIDL release).
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