A comprehensive assessment of inbreeding and laboratory adaptation in Aedes aegypti mosquitoes

Abstract

Modified Aedes aegypti mosquitoes reared in laboratories are being released around the world to control wild mosquito populations and the diseases they transmit. Several efforts have failed due to poor competitiveness of the released mosquitoes. We hypothesized that colonized mosquito populations could suffer from inbreeding depression and adapt to laboratory conditions, reducing their performance in the field. We established replicate populations of Ae. aegypti mosquitoes collected from Queensland, Australia, and maintained them in the laboratory for twelve generations at different census sizes. Mosquito colonies maintained at small census sizes (≤100 individuals) suffered from inbreeding depression due to low effective population sizes which were only 25% of the census size as estimated by SNP markers. Populations that underwent full-sib mating for nine consecutive generations had greatly reduced performance across all traits measured. We compared the established laboratory populations with their ancestral population resurrected from quiescent eggs for evidence of laboratory adaptation. The overall performance of laboratory populations maintained at a large census size (400 individuals) increased, potentially reflecting adaptation to artificial rearing conditions. However, most individual traits were unaffected, and patterns of adaptation were not consistent across populations. Differences between replicate populations may indicate that founder effects and drift affect experimental outcomes. Though we find limited evidence of laboratory adaptation, mosquitoes maintained at low population sizes can clearly suffer fitness costs, compromising the success of "rear-and-release" strategies for arbovirus control.

Keywords: Aedes aegypti; biological control; colonization; inbreeding; laboratory adaptation.

Figure 1

Maintenance scheme for replicate Aedes aegypti laboratory populations. An ancestral population was established from eggs collected from Townsville, Australia, that all other populations were derived from. Replicate populations were maintained separately beginning from F₂ and were not interbred

Figure 2

Development time of Aedes aegypti F₁₃ laboratory populations maintained at different census sizes. Mean development time was measured for (a&c) female and (b&d) male larvae under (a&b) high nutrition (food provided ad libitum) and (c&d) low nutrition (0.1 mg of TetraMin^® per larva every 2 days) conditions. Each data point represents the mean development time of individuals from a single container of 100 larvae. Inbred lines B and C were not tested under low nutrition conditions. The dashed line represents the mean development time of the Townsville F_4/5 ancestral population. Error bars are standard deviations

Figure 3

Survival to adulthood of Aedes aegypti F₁₃ laboratory populations maintained at different census sizes. The percentage of larvae surviving to adulthood was tested under (a) high nutrition (food provided ad libitum) and (b) low nutrition (0.1 mg of TetraMin^® per larva every 2 days) conditions. Solid black lines indicate the median survival of each population. The dashed line represents the median survival of the Townsville F_4/5 ancestral population

Figure 4

Fecundity (a) and egg hatch proportions (b) of Aedes aegypti F₁₃ laboratory populations maintained at different census sizes. Fifteen females were tested per line, or as many as possible for inbred lines B and C. The dashed line represents the mean fecundity (a) or median egg hatch proportion (b) of the Townsville F_4/5 ancestral population. Solid black lines indicate the mean fecundity (a) or median egg hatch proportion (b) of each population. Error bars are standard deviations

Figure 5

Relative performance of Aedes aegypti F₁₃ laboratory populations maintained at different census sizes. Each data point represents the performance index of a single replicate population relative to the ancestral population (Townsville F_4/5) which is represented by the black dotted line. Black bars indicate means and standard deviations

Figure 6

Relative mating success of Aedes aegypti males maintained in the laboratory for different numbers of generations. We tested the relative mating success of males from Cairns F₂, F₇, and F₂₇ populations when competing against Wolbachia‐infected males for access to Cairns F₂ females. An inbred colony (Inbred A F₁₈) was included for comparison. Higher hatch proportions indicate increased mating success of the experimental males relative to Wolbachia‐infected males. Each data point represents the mean egg hatch proportion from a cage of 50 females. Black bars indicate means and standard deviations