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. 2014 May;7(5):597-606.
doi: 10.1111/eva.12159. Epub 2014 May 1.

Population-level effects of fitness costs associated with repressible female-lethal transgene insertions in two pest insects

Tim Harvey-Samuel  1 , Thomas Ant  1 , Hongfei Gong  2 , Neil I Morrison  2 , Luke Alphey  1
Affiliations

Population-level effects of fitness costs associated with repressible female-lethal transgene insertions in two pest insects

Tim Harvey-Samuel et al. Evol Appl. 2014 May.

Abstract

Genetic control strategies offer great potential for the sustainable and effective control of insect pests. These strategies involve the field release of transgenic insects with the aim of introducing engineered alleles into wild populations, either permanently or transiently. Their efficacy can therefore be reduced if transgene-associated fitness costs reduce the relative performance of released insects. We describe a method of measuring the fitness costs associated with transgenes by analyzing their evolutionary trajectories when placed in competition with wild-type alleles in replicated cage populations. Using this method, we estimated lifetime fitness costs associated with two repressible female-lethal transgenes in the diamondback moth and olive fly as being acceptable for field suppression programs. Furthermore, using these estimates of genotype-level fitness costs, we were able to project longer-term evolutionary trajectories for the transgenes investigated. Results from these projections demonstrate that although transgene-associated fitness costs will ultimately cause these transgenes to become extinct, even when engineered lethality is repressed, they may persist for varying periods of time before doing so. This implies that tetracycline-mediated transgene field persistence in these strains is unlikely and suggests that realistic estimates of transgene-associated fitness costs may be useful in trialing 'uncoupled' gene drive system components in the field.

Keywords: fitness costs; genetic engineering; insect; integrated pest management; release of insects carrying a dominant lethal; transgenic.

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Figures

Figure 1
Figure 1
Mean transgene and wild-type allele frequencies (±SE) tracked over 10 generations in three and two mixed populations of diamondback moth (A) and olive fruit fly (B) containing the fsRIDL transgene insertions OX4319L-Pxy and OX3097D-Bol, respectively. Allele frequencies were estimated by genotyping 96 randomly chosen adults per population, per generation, for both the transgene insertion and the corresponding no-insertion wild-type allele. Triangles and circles represent the mean frequencies of the transgene (R) and wild-type (–) allele recorded in each generation, respectively.
Figure 2
Figure 2
(A) Mean frequencies (±SE) of transgenic homozygous (R/R, triangles), heterozygous (R/–, circles), and wild type (–/–, squares) in two and three mixed-genotype populations of diamondback moth (upper panel) and olive fly (lower panel), respectively. Diamondback moth populations were established with 100 homozygous transgenic male and 100 heterozygous transgenic female insects. Olive fly populations were established with 100 heterozygous transgenic male and 100 heterozygous transgenic female insects. Experimental populations were observed for 10 generations. Engineered female lethality was suppressed throughout the experiment by provision of dietary tetracycline, and population size was maintained at 200 adults in each generation. (B) Relative fitness values for –/–, R/– and R/R genotypes (±SE) of OX4319L-Pxy (upper panel) and OX3097D-Bol (lower panel) calculated from corrected rate of increase parameters with values relative to the –/– genotype. Relative fitness values were WR/R = 0.477, WR/– = 0.736, and W–/– = 1 for diamondback moth and WR/R = 0.975, WR/– = 0.974, and W–/– = 1 for olive fly. (C) Results of a deterministic population genetics model illustrating theoretical genotype trajectories in mixed-genotype populations of diamondback moth (upper panel) and olive fly (lower panel) using the experimentally derived mean estimated relative fitness values from (B). Note that model outputs represent more generations than the cage experiment, to illustrate longer-term trajectories.
Figure 3
Figure 3
Boxplots showing results from 250 iterations of a stochastic model simulating engineered female-specific selection on a fsRIDL allele in a panmictic, closed population of constant size over 15 discrete generations. We consider fsRIDL allele frequency with a starting population of 200 individuals and an initial fsRIDL allele frequency of 0.25 (f = 0.25) propagating in the absence of the transgene repressor (under restrictive conditions). Horizontal bold lines represent generational medians; upper and lower box lines represent first and third quartiles, respectively; outer horizontal lines represent 1.5× the interquartile range; and dots represent data points over 1.5× above or below the first and third quartiles, respectively. Overlaid onto the boxplots are lines (red, blue and green) showing allele frequency changes from three replicates of caged experiments tracking fsRIDL allele frequencies in mixed populations of (A) diamondback moth and (B) olive fly reared under analogous conditions to those used in the model (initial fsRIDL allele frequency of 0.25, restrictive conditions).
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