The Trojan female technique: a novel, effective and humane approach for pest population control

Abstract

Humankind's ongoing battle with pest species spans millennia. Pests cause or carry disease, damage or consume food crops and other resources, and drive global environmental change. Conventional approaches to pest management usually involve lethal control, but such approaches are costly, of varying efficiency and often have ethical issues. Thus, pest management via control of reproductive output is increasingly considered an optimal solution. One of the most successful such 'fertility control' strategies developed to date is the sterile male technique (SMT), in which large numbers of sterile males are released into a population each generation. However, this approach is time-consuming, labour-intensive and costly. We use mathematical models to test a new twist on the SMT, using maternally inherited mitochondrial (mtDNA) mutations that affect male, but not female reproductive fitness. 'Trojan females' carrying such mutations, and their female descendants, produce 'sterile-male'-equivalents under natural conditions over multiple generations. We find that the Trojan female technique (TFT) has the potential to be a novel humane approach for pest control. Single large releases and relatively few small repeat releases of Trojan females both provided effective and persistent control within relatively few generations. Although greatest efficacy was predicted for high-turnover species, the additive nature of multiple releases made the TFT applicable to the full range of life histories modelled. The extensive conservation of mtDNA among eukaryotes suggests this approach could have broad utility for pest control.

Keywords: biocontrol; fertility control; mathematical model; mtDNA; population viability; sterile male technique.

Figure 1.

(a–c) Contour plots of relative population decline predicted for pests across birth/death rate parameter space (with a set generation time of 12 months), following single or repeated releases of TFs. All rates are yearly. The white region in (a–c) corresponds to parameter space where the death rate exceeds the birth rate. (a) Single release of 1% standing population. (b) Single release of 10% standing population. (c) Multiple releases of 1% per year for 10 consecutive years. (d) The relationship between the total declines achieved versus the number of successive years of releasing TFs at 1% per annum. Blue solid line: birth rate = 2 per year; death rate = 1 per year. Red dashed lines: birth rate = 8 per year; death rate decreases from left to right (5, 3, 1).

Figure 2.

Comparison of the SMT (red) and the TFT (blue) at their minimum yearly release rates sufficient to suppress the modelled population to 1% of its initial level within 10 years (with birth rate = 8 per year and death rate = 1 per year). The comparable yearly release rates of SMs and TFs were 65% and 22% of the standing population, respectively.

Figure 3.

The effect of female multiple mating on the predicted efficiency of the TFT for 10 successive yearly releases of TFs at 1% of the standing population. Each line shows the population suppression achieved, for populations with different yearly per capita birth/death rates, as the number of mating partners a female has during the mating season increases.