Field detection and predicted evolution of spinosad resistance in Ceratitis capitata

Abstract

BACKGROUND: The sustainable control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), is compromised by the development of resistance to malathion and lambda-cyhalothrin in Spanish field populations. At present, field populations remain susceptible to spinosad. However, the resistant strain JW-100s has been obtained under laboratory selection with spinosad, and resistance has been associated with the presence of different mutations causing truncated transcripts of the ⊍6 subunit of the nicotinic acetylcholine receptor (nAChR⊍6). RESULTS: An F1 screen assay followed by the molecular characterization of surviving flies has been used to search for spinosadresistant alleles in field populations. Two different resistant alleles giving rise to truncated isoforms of Cc⊍6 have been identified, which corresponds to an estimated allelic frequency of at least 0.0023-0.0046. The fitness values of the resistant nAChR⊍6 alleles found in the laboratory strain JW-100s were estimated to be 0.4 for RR and 0.2 for SR. Mathematical modelling predicted that spinosad-resistant alleles will rapidly decline over time in field populations if their fitness cost was the same as estimated for laboratory-resistant alleles. However, they are predicted to increase in the field if their fitness cost is lower and resistance management strategies are not implemented. CONCLUSION: Spinosad-resistant alleles have been detected in field populations for the first time. Our modelling simulations indicate that the best option to delay the appearance of spinosad resistance would be its rotation with other insecticides without cross-resistance. The integrated F1 screen/molecular genetic analysis presented here can be used for future monitoring studies.

Current situation and forecasting of resistance evolution to lambda‐cyhalothrin in Spanish medfly populations

“…7 Modeling performed by our group predicted that, if the fitness cost of field resistant individuals is equivalent to that estimated for resistant laboratory strains, the resistant alleles would rapidly decline over time resulting in the disappearance of spinosad resistant individuals from the field populations. 7 Nonetheless, if field-evolved spinosad resistance is associated with a low fitness cost, resistant individuals would be expected to rise in the field. A recent study did not reveal significant levels of resistance of field populations to deltamethrin and spinosad in Greece.…”

“…These values are lower than those estimated for the fitness cost associated with genotypes carrying spinosad resistant alleles in C. capitata (0.4 for RR and 0.2 for RS), obtained in a study of their stability when in competition with individuals carrying the wildtype alleles under laboratory conditions. 7 These fitness cost values may be related to the trade-offs in life-history and behavioral traits reported, respectively, for lambda-cyhalothrin 13 and spinosad resistance, 27 but the distinct methodologies used for their estimation does not allow direct comparisons. Another aspect that may have an impact on the evolution of resistance is its type of inheritance.…”

Inheritance, Fitness Cost, and Management of Lambda-Cyhalothrin Resistance in a Laboratory-Selected Strain of Ceratitis capitata (Wiedemann)

“…Nonetheless, susceptibility to lambda-cyhalothrin sharply increased when treating with spinosad because (1) recessive susceptible alleles remain in the populations carried by heterozygotes, and (2) the alterations observed for some biological traits in lambda-cyhalothrin-resistant individuals may convey a fitness cost that contributes to the instability of lambda-cyhalothrin resistance. In the case of spinosad, a predictive model developed by our group aimed at the intensive and sole use of this insecticide could result in an increase in the frequency of spinosad-resistant alleles [ 4 ]. Although our simulation study started with a higher frequency of spinosad-resistant alleles than the above-mentioned model, it reinforced the idea that even though the recessive nature of spinosad resistance makes its evolution slow at the beginning, the spread of resistance can be very fast when resistant individuals are abundant in the population.…”

“…However, the sustainability of management programs and the durability of available insecticides are threatened by the evidence of field-evolved resistance to malathion [ 2 ] and lambda-cyhalothrin [ 3 ]. Moreover, although medfly susceptibility to spinosad remains, resistant alleles for this insecticide have recently been discovered in field populations [ 4 ]. In this context, the implementation of Insecticide Resistance Management (IRM) strategies aimed at either overcoming resistance to currently used compounds or preventing the development of resistance to extant or new insecticides becomes essential [ 5 , 6 ].…”

“…Remarkably, the lambda-cyhalothrin-resistant W-1Kλ strain showed high levels of cross-resistance to deltamethrin but not to spinosad [ 3 ], which suggests that it would be advisable for medfly control to rotate lambda-cyhalothrin and spinosad. In a previous study, a resistance evolutionary model based on empirical data on spinosad resistance in medfly (inheritance, fitness cost, and frequency of resistant alleles in the field) led us to conclude that rotations with spinosad and an insecticide from a different chemical family would help manage the development of resistance [ 4 ]. However, a similar approach to investigate how lambda-cyhalothrin resistance could evolve has not been explored, because most of the required parameters are unknown.…”