Alternative patterns of sex chromosome differentiation in Aedes aegypti (L)

Abstract

Background: Some populations of West African Aedes aegypti, the dengue and zika vector, are reproductively incompatible; our earlier study showed that divergence and rearrangements of genes on chromosome 1, which bears the sex locus (M), may be involved. We also previously described a proposed cryptic subspecies SenAae (PK10, Senegal) that had many more high inter-sex F_ST genes on chromosome 1 than did Ae.aegypti aegypti (Aaa, Pai Lom, Thailand). The current work more thoroughly explores the significance of those findings.

Results: Intersex standardized variance (F_ST) of single nucleotide polymorphisms (SNPs) was characterized from genomic exome capture libraries of both sexes in representative natural populations of Aaa and SenAae. Our goal was to identify SNPs that varied in frequency between males and females, and most were expected to occur on chromosome 1. Use of the assembled AaegL4 reference alleviated the previous problem of unmapped genes. Because the M locus gene nix was not captured and not present in AaegL4, the male-determining locus, per se, was not explored. Sex-associated genes were those with F_ST values ≥ 0.100 and/or with increased expected heterozygosity (H _exp , one-sided T-test, p < 0.05) in males. There were 85 genes common to both collections with high inter-sex F_ST values; all genes but one were located on chromosome 1. Aaa showed the expected cluster of high inter-sex F_ST genes proximal to the M locus, whereas SenAae had inter-sex F_ST genes along the length of chromosome 1. In addition, the Aaa M-locus proximal region showed increased H _exp levels in males, whereas SenAae did not. In SenAae, chromosomal rearrangements and subsequent suppressed recombination may have accelerated X-Y differentiation.

Conclusions: The evidence presented here is consistent with differential evolution of proto-Y chromosomes in Aaa and SenAae.

Keywords: Arbovirus vector; Dimorphic traits; Evolution of reproductive proteins; Genomics; Population genetics; Sex determination.

Fig. 1

Inter-sex F_ST values vary among A.aegypti populations. Relative position of gene-wise F_ST values per chromosome. Red dots indicate genes with F_ST values ≥ 0.100 (Aaa, (Thai) collection, n = 304; SenAae (PK10) n = 1310); black dots indicate F_ST values below the threshold. Blue carat indicates predicted location of nix at the M locus

Fig. 2

Inter-sex H_exp values vary among A.aegypti populations. Relative position of gene-wise H_exp values for those genes in the high F_ST group (F_ST ≥ 0.100). Red dots indicate male gene-wise H_exp values; black dots indicate female gene-wise H_exp values. Blue carat indicates predicted location of nix at the M locus

Fig. 3

Functional categories of genes showing sex-specific polymorphisms. a The intersection of genes among both populations with high inter-sex F_ST values (≥ 0.100). b The resulting 85 common genes were classified by functional category and are shown as a portion of the pie chart. Legend: the list of functional groups, arranged from top to bottom, is represented in the pie chart clock-wise, starting at the top-most slice