Local adaptation ofAedes aegyptimosquitoes toWolbachia-induced fitness costs

Abstract

Aedes aegypti mosquito eggs can remain quiescent for many months before hatching, allowing populations to persist through unfavorable conditions. Aedes aegypti infected with the Wolbachia strain wMel have been released in tropical and subtropical regions for dengue control. wMel reduces the viability of quiescent eggs, but this physiological cost might be expected to evolve in natural mosquito populations that frequently experience stressful conditions. We therefore compared the costs of wMel infection for quiescent egg viability in field-derived and laboratory populations. Quiescent egg viability was highly variable in wMel-infected populations, with greater costs of wMel in field-derived populations. In contrast, there was little variation between matched field-derived and long-term laboratory populations lacking wMel, suggesting that laboratory adaptation does not influence this trait and that differences are due to wMel infection. Comparisons of populations collected a year apart show a decline in costs under laboratory rearing conditions involving a rapid turnover of mosquito generations; this pattern was consistent across populations despite their origin, suggesting adaptation of mosquitoes to the wMel infection under laboratory conditions. Reciprocal crossing experiments confirm that differences in quiescent egg viability were mainly due to the genetic background and not Wolbachia alone. wMel-infected mosquitoes hatching from long-term quiescent eggs showed partial loss of cytoplasmic incompatibility and female infertility, highlighting additional costs of long-term quiescence. Our study provides the first evidence for a shift in Wolbachia phenotypic effects following deliberate field release and establishment and it highlights interactions between Wolbachia infections and local adaptation. The unexpected changes in fitness costs observed here suggest potential tradeoffs with undescribed fitness benefits of the wMel infection.

Wolbachia inhibits ovarian formation and increases blood feeding rate in female Aedes aegypti

“…aegypti eggs, we discovered a novel reproductive effect induced by w AlbB, in which infected females that hatched from quiescent eggs were infertile despite successful mating and the proportion of females showing infertility was correlated with the duration of egg quiescence [ 23 ]. The w Mel strain also causes female infertility following egg storage, but to a lesser extent than w AlbB [ 23 , 24 ]. Several other reproductive fitness costs of Wolbachia , including those on the number and viability of eggs, can be attributed to the consequence of nutritional competition between Wolbachia and its host [ 25 ] and represent quantitative effects.…”

Wolbachiainhibits ovarian formation and increases blood feeding rate in femaleAedes aegypti

“…aegypti eggs, we discovered a novel reproductive effect induced by w AlbB, in which infected females that hatched from quiescent eggs lost their fertility despite successful mating, with the proportion of female infertility being correlated with the duration of egg quiescence [20]. The w Mel strain also causes female infertility following egg storage, but to a lesser extent than w AlbB [20, 21]. Several other reproductive fitness costs of Wolbachia , including those on the number and viability of eggs, can be attributed to the consequence of nutritional competition between Wolbachia and its host [22] and represent quantitative effects.…”

Differences in gene expression in field populations ofWolbachia-infectedAedes aegyptimosquitoes with varying release histories in northern Australia

“…Hence, some analysis of the type and function of DEGs not common to all the release groups is warranted but is only discussed briefly below. Finally, as Aae.wMel 2017 mosquitoes had significantly higher numbers of both up- and down-regulated DEGs compared with the other release years, the gene expression changes in that group will also be discussed to help understand this observation which may be related to ongoing host evolution of Wolbachia mediated effects [27].…”

“…Furthermore, although we show different gene expression profiles between different release dates, future sampling should be conducted in other global release locations, such as Yogyakarta [16] or Kuala Lumpur [9], to examine whether geographically separate local release sites show geographical and temporal differences in gene expression. Changes in gene expression related to other processes, such as the shift in quiescence patterns [27], also require further study.…”

“…In recent studies to explore the first possibility, mosquitoes collected from north Queensland had few changes in their Wolbachia genome sequences compared to the pre-release strain, indicating a high level of stability to date [23, 24]. In addition, a comparison of the mosquito genomes also suggests that there have been few changes in the mosquito genome since Wolbachia replacement [25], whilst the frequency of Wolbachia in invaded populations has remained high [14, 26] and most host effects of the Wolbachia have remained stable [26] with the exception of effects on egg quiescence [27]. Although few genomic changes have so far been detected and linked to structural changes in genes, it is possible that there have nevertheless been changes in the expression of host genes which are often sensitive indicators of adaptation, including in immune responses [28].…”