Irradiation dose does not affect male reproductive organ size, sperm storage, and female remating propensity in Ceratitis capitata

Abstract

The Mediterranean fruit fly Ceratitis capitata is a globally invasive pest, often controlled with the sterile insect technique (SIT). For the SIT, mass-rearing of the target insect followed by irradiation are imperatives. Sterile males are often less able to inhibit female remating and transfer less number of sperm, and even irradiation could affect male reproductive organs, with consequences for their ability to inhibit female remating. On the other hand, male age could affect their ability to modulate female response after mating. Here, we evaluated the quality of the genetic sexing strain Vienna-8-tsl mass-reared in Bioplanta San Juan, Argentina, under laboratory conditions, with regard to: (i) the ability of sterile males irradiated at 100 or 140 Gy to inhibit female remating, in the same day and at 24 h of first copulation; (ii) the ability of 3, 4 or 5 day-old sterile males to inhibit female remating at 24 h of first copulation, and (iii) the effect of a reduction in irradiation doses on the number of sperm stored by females and reproductive organ size in virgin males. Sterile males were better able than wild males to inhibit female remating in the same day of first copulation and as able as wild males 1 day after first copulation. Male age did not affect their ability to inhibit female receptivity. Number of sperm stored by females, testes size and ectodermal accessory glands size were not affected by male identity, while sterile 100 Gy males had larger mesodermal accessory glands than control lab males. A reduction in irradiation dose does not impact any variable measured, except for percentage of sperm-depleted females: females mated with sterile 100 Gy males had lower probabilities to store sperm. The results showed here are very encouraging for tsl Vienna 8 strain reared in Argentina and are discussed in comparison with previous studies in C. capitata female remating with dissimilar results.

On the impact of re-mating and residual fertility on the Sterile Insect Technique efficacy: case study with the medfly, Ceratitis capitata

“…Although lifespan is difficult to estimate in the field, one can consider that sterile males are only useful as long as they can inseminate wild females. However, Abraham et al [25] showed that sperm-depleted sterile males would still be able to transfer accessory gland substances that would trigger a refractory behavior in females.…”

“…Sterile Queensland flies were reported to have a maximum of 2 or 3 mating capacity [67]; however, even depleted, they were able to copulate and to induce refractoriness in females. Studies have shown that the injection of male accessory gland substances was able to induce refractoriness in Queensland flies, but also in medflies [25, 68]. Costa et al [65] showed that a lower quantity of sperm transferred would increase the chances of re-mating in females.…”

“…Some field studies reported percentages of double mating in wild females: up to 50% [10]; < 28% [12]; 4 to 28% [26]. Laboratory tests reported by Abraham et al [1] indicated 20% re-mating for females mated with 100Gy-irradiated males. Recently, Pogue et al (2022)have shown that female mating propensity reduces over time [41]: with an average of 75% females C.capitata re-mating a second time but only less than 25% performing successive re-mating.…”

“…The tolerable value for residual fertility is very low according to the chosen parameters values. This would give reason to SIT implementation programs that choose a fully sterilizing dose, such as [1]. In the following simulations, we consider RF values varying from 0 to 0.9%.…”

“…Residual fertility is easy to assess and is part of the quality control of every SIT program (interested readers are referred to the manual published by the International Atomic Energy Agency (IAEA) [24] for medfly SIT procedures). For C. capitata , a dose of 140Gy is required to achieve full sterility, as in the medfly management program in Argentina [25]; however, this dosage can also negatively affect male performance and therefore be detrimental for SIT operations [26, 27]. On the other hand, in an ongoing operational SIT program against medflies in the region of Valencia, Spain, the induced average sterility reached 98.87 ± 0.55% with an irradiation dose of 100 Gy, leading to a residual fertility of 1.13 ± 0.55% [5].…”