1. Genetics and Genomics
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Introduction of a male-harming mitochondrial haplotype via ‘Trojan Females’ achieves population suppression in fruit flies

  1. Jonci Nikolai Wolff  Is a corresponding author
  2. Neil J Gemmell
  3. Daniel M Tompkins
  4. Damian K Dowling
  1. Monash University, Australia
  2. University of Otago, New Zealand
  3. Landcare Research, New Zealand
Research Article
Cite this article as: eLife 2017;6:e23551 doi: 10.7554/eLife.23551
4 figures and 5 tables

Figures

Mean offspring number and haplotype frequencies under density-controlled population conditions (Experiment 1).

(A) Mean offspring number (±SEM), and B) mean haplotype frequencies (±SEM) of experimental populations in Experiment 1 over 10 generations, under density-controlled conditions. Founding populations (F0) were established with varying proportions (0%, 25%, 50%, 75%) of the TFT haplotype. Each generation was propagated with 80 eggs. Genotyping was conducted at generations 1, 5, and 10.

https://doi.org/10.7554/eLife.23551.006
Figure 1—source data 1

Raw data for offspring number and TFT frequency for Experiment 1.

Offspring numbers per population for each of 10 generations and TFT frequencies for each population at generations 1, 5 and 10.

https://doi.org/10.7554/eLife.23551.007
Mean offspring number in relation to TFT haplotype frequency under density-controlled (Experiment 1) and fluctuating population conditions (Experiment 2).

Mean offspring number (±SEM) across experimental populations (A–C) with regulated population size at generations 1, 5, and 10 in Experiment 1; and (D) with fluctuating population size at generation 10 in Experiment 2. Haplotype frequencies were determined by genotyping seven females for each experimental population at each of three generations (1, 5, and 10; n = 1323) in Experiment 1; and by genotyping nine females for each experimental population at generation 10 (n = 567) in Experiment 2.

https://doi.org/10.7554/eLife.23551.009
Figure 2—source data 1

Raw data for offspring number and TFT frequency for Experiments 1 and 2.

Offspring numbers per population for each of 10 generations in Experiment 1 and 2. TFT frequencies for each population at generations 1, 5 and 10 for Experiment 1 and at generation 10 for Experiment 2.

https://doi.org/10.7554/eLife.23551.010
Mean offspring number and haplotype frequencies under fluctuating population conditions (Experiment 2).

Mean offspring number (±SEM, on vertical axis on left-hand side), and mean haplotype frequencies (±SEM, right-hand side) at generation 10, of experimental populations. Founding populations (F0) were established with varying proportions (0%, 25%, 50%, 75%) of fruit fly pairs harboring the mt:Cyt-b TFT mutation. Each generation, each experimental population was propagated with all offspring of the previous generation.

https://doi.org/10.7554/eLife.23551.011
Figure 3—source data 1

Raw data for offspring number and TFT frequency for Experiment 2.

Offspring numbers per population for each of 10 generations and TFT frequency for each population at generation 10.

https://doi.org/10.7554/eLife.23551.012
Experimental breeding scheme.

The TFT-bearing BRO haplotype and the putatively healthy DAH haplotype were introgressed into the outbred nuclear background Dahomey in three independent replicates (i.e. BRO:Dahomey1-3; DAH:Dahomey1-3). Experimental populations were established by supplementing DAH:Dahomey test populations (DAH:Dahomey1-3) with varying contributions of fly pairs bearing the TFT haplotype (0%, 25%, 50%, 75%) sourced from the corresponding BRO:Dahomey replicate population (i.e. DAH:Dahomey1/BRO:Dahomey1; DAH:Dahomey2/BRO:Dahomey2; DAH:Dahomey3/BRO:Dahomey3). For each of the three biological replicates and for each treatment class (0%, 25%, 50%, 75%), we established seven technical replicate populations. These experimental populations were further duplicated, one cohort providing populations for the regulated population size approach (Experiment 1), and one cohort for the fluctuating population size approach (Experiment 2).

https://doi.org/10.7554/eLife.23551.015

Tables

Table 1

Mean offspring numbers, TFT haplotype frequencies, and genotyping outcomes for the two experiments (regulated conditions and fluctuating conditions).

https://doi.org/10.7554/eLife.23551.003
TFT treatment (starting frequency)0% TFT25% TFT50% TFT75% TFT
Populations [n]21212121
ExperimentRegulatedF1 Frequency0.000.26 ± 0.030.44 ± 0.030.63 ± 0.03
F5 Frequency0.000.15 ± 0.030.63 ± 0.030.71 ± 0.02
F10 Frequency0.000.17 ± 0.030.67 ± 0.030.80 ± 0.03
Loss-400
Fixation-003
Heteroplasmy-000
Mean offspring number (F10)74.15 ± 1.0072.05 ± 0.8967.43 ± 0.9966.38 ± 0.70
Population extinction1000
FluctuatingF10frequency0.000.35 ± 0.060.59 ± 0.060.75 ± 0.05
Loss-410
Fixation-144
Heteroplasmy-020
Mean offspring number (F10)80.47 ± 5.1281.19 ± 4.5978.56 ± 5.6385.86 ± 3.73
Population extinction2020
Table 1—source data 1

Raw data for offspring number and TFT frequency for Experiments 1 and 2.

Offspring number per population for each of 10 generations in Experiment 1 and 2. TFT frequency for each population at generations 1, 5 and 10 for Experiment 1 and at generation 10 for Experiment 2.

https://doi.org/10.7554/eLife.23551.004
Table 2

(A) Linear mixed model showing effects of TFT treatment and generation number on mean offspring number, and (B) generalized linear mixed model of effects of TFT treatment and generation on TFT haplotype frequency of populations with regulated population size (Experiment 1). There was no evidence of overdispersion in the model of TFT haplotype frequency (dispersion parameter = 0.766), and addition of an observation-level random effect to the final model did not change this parameter (dispersion parameter = 0.767), nor the parameter estimates of the model.

https://doi.org/10.7554/eLife.23551.005
(A) Offspring number(B) TFT frequency
Fixed effectsχ2Dfpχ2Dfp
TFT treatment2.2330.5338.142<0.001
Generation14.7390.106.2120.045
TFT treatment × generation51.09270.00323.524<0.001
Random effectsSD*SD*
Biological replicate0.81--0--
Experimental population1.11--0--
Residual5.48-----
* Standard deviation
Table 3

Linear mixed model of association of TFT haplotype frequency on mean offspring number in populations with regulated population size (Experiment 1).

https://doi.org/10.7554/eLife.23551.008
Fixed effectsχ2DfP
TFT frequency21.3770.003
Random effectsSD*
Biological replicate0.31--
Experimental population0--
Generation2.77--
Residual6.40--
* Standard deviation
Table 4

(A) Linear mixed model showing effects of TFT treatment and generation on mean offspring number; and (B) generalized linear mixed model of effects of TFT treatment on TFT haplotype frequency of populations with fluctuating population size (Experiment 2). When reanalyzing mean offspring number (A), having excluded the 15 zero values in the dataset resulting from three vial extinctions (two from the TFT 0% treatment, and one from the TFT 50% treatment), the effect of TFT treatment on offspring number remained statistically non-significant (χ2=3.2, p=0.36). The binomial model of TFT frequency (b) indicated overdispersion (overdispersion parameter = 1.85), and thus an observation-level random effect was added (experimental population) to the model (overdispersion parameter of final model = 1.07).

https://doi.org/10.7554/eLife.23551.013
(A) Offspring number(B) TFT frequency
Fixed effectsχ2DfP2DfP
TFT treatment4.9830.1720.332<0.001
Generation46.729<0.001---
Random effectsSD*




Biological replicate3.1--0--
Experimental population11.2--1.32--
Residual20.85-----
* Standard deviation
Table 5

Linear model of association of TFT haplotype frequency on mean offspring number in populations with fluctuating population size (Experiment 2).

https://doi.org/10.7554/eLife.23551.014
Fixed effectsχ2DfP
TFT Frequency4.9590.839
Random effectsSD*
Biological replicate0--
Residual24.93--
* Standard deviation

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