Adaptation to Aridity in the Malaria Mosquito Anopheles gambiae: Chromosomal Inversion Polymorphism and Body Size Influence Resistance to Desiccation

Abstract

Chromosomal inversions are thought to confer a selective advantage in alternative habitats by protecting co-adapted alleles from recombination. The frequencies of two inversions (2La and 2Rb) of the afro-tropical malaria mosquito Anopheles gambiae change gradually along geographical clines, increasing in frequency with degree of aridity. Such clines can result from gene flow and local selection acting upon alternative karyotypes along the cline, suggesting that these inversions may be associated with tolerance to xeric conditions. Since water loss represents a major challenge in xeric habitats, it can be supposed that genes inside these inversions are involved in water homeostasis. To test this hypothesis, we compared the desiccation resistance of alternative karyotypes from a colonised 2Rb/2La polymorphic population of A. gambiae from Cameroon. The strain included only the molecular form S, one of the genetic units marking incipient speciation in this taxon. Day-old mosquitoes of both sexes were assayed individually for time to death in a dry environment and the karyotype of each was determined post-mortem using molecular diagnostic assays for each inversion. In agreement with expectations based on their eco-geographical distribution, we found that 2La homokaryotypes survived significantly longer (1.3 hours) than the other karyotypes. However, there was weak support for the effect of 2Rb on desiccation resistance. Larger mosquitoes survived longer than smaller ones. Median survival of females was greater than males, but the effect of sex on desiccation resistance was weakly supported, indicating that differential survival was correlated to differences between sexes in average size. We found weak evidence for a heterotic effect of 2La karyotype on size in females. These results support the notion that genes located inside the 2La inversion are involved in water balance, contributing towards local adaptation of A. gambiae to xeric habitats, beyond the adaptive value conferred by a larger body size.

Ecophysiology of Anopheles gambiae s.l.: Persistence in the Sahel

“…In a subsequent study, using 1-day-old mosquitoes representing different karyotypes within An. gambiae s.s. (previously the S molecular form), 2La-homozygotes exhibited higher desiccation tolerance than the standard-homozygotes (612 vs. 537 min or 13%), although the heterozygotes exhibited apparently lower resistance than both (529 min; Fouet et al, 2012; Table 1). Notably, body size of the 2La-homozygotes was larger than that those carrying the standard karyotype, but the heterozygotes were apparently the largest (Fouet et al, 2012).…”

“…gambiae s.s. (previously the S molecular form), 2La-homozygotes exhibited higher desiccation tolerance than the standard-homozygotes (612 vs. 537 min or 13%), although the heterozygotes exhibited apparently lower resistance than both (529 min; Fouet et al, 2012; Table 1). Notably, body size of the 2La-homozygotes was larger than that those carrying the standard karyotype, but the heterozygotes were apparently the largest (Fouet et al, 2012). The difference was only found in teneral mosquitoes and no difference was detected after 1 day posteclosion (Fouet et al, 2012).…”

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

“…3A-C). In principle, the north-south structuring could be caused solely by differences in chromosome 2 inversion frequencies, which form a cline from near absence in the humid south to fixation in the arid north Fouet et al 2012). However, we find SNPs from all five chromosomal arms consistently separate northern and southern mosquitoes, indicating a substantial genome-wide divergence between the two populations (supplementary fig.…”

Novel insights into the metabolic and biochemical underpinnings assisting dry-season survival in female malaria mosquitoes of the Anopheles gambiae complex

“…Survival under desiccating conditions was assessed in females of both the M and S molecular forms reared under ''rs'' and ''ods'' environmental conditions, using previously described protocols (Fouet et al, 2012;Gray et al, 2009). Twenty-four hour old females were supplied with water for the first 12 h, and were individually placed into plastic vials (28.5 mm diameter  95 mm height) filled with 3 cm of desiccant (Silica gel ChameleonÓ), a piece of cotton to avoid the direct contact between the mosquito and the desiccant, and sealed with a plastic film (ParafilmÓ).…”