Exon-Enriched Libraries Reveal Large Genic Differences Between Aedes aegypti from Senegal, West Africa, and Populations Outside Africa

Abstract

Aedes aegypti is one of the most studied mosquito species, and the principal vector of several arboviruses pathogenic to humans. Recently failure to oviposit, low fecundity, and poor egg-to-adult survival were observed when Ae. aegypti from Senegal (SenAae) West Africa were crossed with Ae. aegypti (Aaa) from outside of Africa, and in SenAae intercrosses. Fluorescent in situ hybridization analyses indicated rearrangements on chromosome 1, and pericentric inversions on chromosomes 2 and 3. Herein, high throughput sequencing (HTS) of exon-enriched libraries was used to compare chromosome-wide genetic diversity among Aaa collections from rural Thailand and Mexico, a sylvatic collection from southeastern Senegal (PK10), and an urban collection from western Senegal (Kaolack). Sex-specific polymorphisms were analyzed in Thailand and PK10 to assess genetic differences between sexes. Expected heterozygosity was greatest in SenAae F_ST distributions of 15,735 genes among all six pairwise comparisons of the four collections indicated that Mexican and Thailand collections are genetically similar, while F_ST distributions between PK10 and Kaolack were distinct. All four comparisons of SenAae with Aaa indicated extreme differentiation. F_ST was uniform between sexes across all chromosomes in Thailand, but were different, especially on the sex autosome 1, in PK10. These patterns correlate with the reproductive isolation noted earlier. We hypothesize that cryptic Ae. aegypti taxa may exist in West Africa, and the large genic differences between Aaa and SenAae detected in the present study have accumulated over a long period following the evolution of chromosome rearrangements in allopatric populations that subsequently cause reproductive isolation when these populations became sympatric.

Keywords: Aedes aegypti; West Africa; genome; population genomics; subspecies.

Figure 1

Expected heterozygosity (H_exp) distribution for each collection. (A) Aaa Mexico (red line), Aaa Thailand (bright blue), SenAae PK-10 (black), and SenAae Kaolack (green). (B) H_exp distributions were compared with one another using a heterogeneity χ² test of the number of genes in each 0.01 bin along the abscissa in the histogram. Aaa vs. SenAae comparisons (red line) have larger LOD differences in H_exp scores than Aaa vs. Aaa (green line) or SenAae vs. SenAae (black line).

Figure 2

(A) Distributions of pairwise F_ST values among all six comparisons of the four collection sites. F_ST values between Aaa collections (red line) are skewed toward smaller values, while F_ST values between SenAae collections (blue line) were generally larger, and shifted to the right. All four F_ST distributions between Aaa and SenAae [i.e., PK10 vs. Mexico (black), PK10 vs. Thailand (green), Kaolack vs. Mexico (tan), and Kaolack vs. Thailand (magenta)] had long right-hand tails, indicating larger F_ST values, and fewer small F_ST values. (B) F_ST distributions were compared with one another using a heterogeneity χ² test of the number of genes in each 0.01 bin along the abscissa in the histogram. The red line is a comparison of F_ST between Aaa [red in (A)] and between SenAae [blue in (A)] with the four F_ST distributions curves [black, green, tan and magenta in (A)] between Aaa and SenAae. The left-hand portion of the red curve indicates a large and significant excess of small F_ST values within the Aaa collection, and within SenAae collections as compared with F_ST values between Aaa and SenAae. The right-hand region of the red curve indicates a large and significant deficiency of large F_ST values within Aaa collections, and within SenAae collections. The blue line in (B) is a comparison of the four Aaa vs. SenAae F_ST distributions (i.e., PK10 vs. Mexico, PK10 vs. Thailand, Kaolack vs. Mexico, and Kaolack vs. Thailand). LOD values are never large, indicating that the four curves are similar. The green line is a comparison of the F_ST distributions within Aaa [red in (A)], and within SenAae [red in (A)]. The left-hand portion of the green curve indicates a large and significant excess of small F_ST values within Aaa collection as compared within SenAae F_ST values. The right hand region of the green curve indicates a large and significant deficiency of large F_ST values within Aaa collections.

Figure 3

Comparison of F_ST values between sexes for genes that have been mapped across the three chromosomes in the PK10 (SenAae) and Thailand (Aaa) collections.

Figure 4

Distribution of F_ST and LOD values between sexes plotted on each chromosome. F_ST distributions were compared with one another using a heterogeneity χ² test of the number of genes in each 0.01 bin along the abscissa in the histogram. (A) F_ST distributions are very similar among all three chromosomes in the Thailand collection. The magenta line indicates the LOD value across the chromosomes, while the black dashed line is the LOD = 3 cutoff. LOD values never exceed the LOD = 3 cutoff. (B) F_ST distributions differ among all three chromosomes in PK10 (SenAae). LOD values across the chromosomes exceed the LOD = 3 cutoff across all three chromosomes.

Figure 5

Average sex-specific F_ST values for SNPs in different regions of a gene. Values were plotted by chromosome in (A) Thailand (Aaa) females vs. males, and (B) PK10 (SenAae) females vs. males.