Polyandrous Mexican Fruit Flies: Second Male Paternity and Biological Attributes of Transgenic Strains

SIMPLE SUMMARY: The Mexican fruit fly is an important pest of certain fruits. As part of its control, the Sterile Insect Technique (SIT) is used. This is an environmentally friendly means of control where insects are mass-reared, sterilized, and then released into areas where the pest is found. Sterile insects are dyed with a fluorescent pigment before release, to distinguish them from the wild population. The efficiency of this technique can be diminished if wild females first mate with a sterile male and then with a wild male. For the Mexican fruit fly, several transgenic strains have been developed that express a fluorescent protein marker for field detection, and are also used as reporters in the creation of strains with complex genetic systems. Here, we report on the biological attributes, mating competitiveness, and the proportion of paternity gained by the second male in twice-mated females with males from two transgenic strains. We found that the males expressing green florescence (443-G) had a better overall performance than the males expressing red fluorescence (419-R). We also found that females produced progeny mostly from the second male to mate with her. This could affect release ratios and diminish the efficiency of the SIT if wild females mate first with a sterile male but remate with a wild male, as she will then lay fertile eggs. These findings are helpful towards delimiting which strains can be used in the future, and determining the proportion of sterile to wild individuals that need to be released in affected areas, for the more efficient control of the Mexican fruit fly. ABSTRACT: Anastrepha ludens (Diptera: Tephritidae), is a damaging agricultural pest. Currently, the Sterile Insect Technique (SIT) is used as part of its control. The SIT consists of the mass-rearing, sterilization, and release of insects in target areas. Sterile males mate with wild females, and prevent them from laying fertile eggs. However, even if females mate with sterile males, they can then remate with a second male. If this second male is wild, then this could reduce the efficiency of the SIT by producing viable offspring. The amount of progeny produced by second males (P2 values) for A. ludens is unknown. Here, we evaluated the biological attributes, mating competitiveness, and the proportion of male paternity gained by the second male, using strains that carry fluorescent marker genes and can be potentially used to develop transgenic sexing strains. Furthermore, the transgenic strains were irradiated, to test their ability to induce sterility in females. We found that the 443-G strain had significantly higher larval survival than the 419-R strain. No significant difference was found between the two strains in their mating probability with wild females. We found P2 values between 67 and 74% for the 419-R and the 443-G strain, respectively. Second male sperm precedence only decreased slightly after 12 days, suggesting that sperm from the first and second male is not mixing with time, but rather the second male’s sperm prevails. Furthermore, sterile 443-G males induced significantly higher sterility in females than sterile males from the 419-R strain. The apparent lower ability of the 443-G strain to inhibit female remating should be further investigated. Knowledge of the pre and postcopulatory performance of transgenic strains will help in understanding their potential for control.