Positive selection near an inversion breakpoint on the neo-X chromosome of Drosophila americana

Abstract

Unique features of heteromorphic sex chromosomes are produced as a consequence of sex-linked transmission. Alternative models concerning the evolution of sex chromosomes can be classified in terms of genetic drift or positive selection being the primary mechanism of divergence between this chromosomal pair. This study examines early changes on a newly acquired chromosomal arm of the X in Drosophila americana, which was derived from a centromeric fusion between the ancestral X and previously autosomal chromosome 4 (element B). Breakpoints of a chromosomal inversion In(4)a, which is restricted to the neo-X, are identified and used to guide a sequence analysis along chromosome 4. Loci flanking the distal breakpoint exhibit patterns of sequence diversity consistent with neutral evolution, yet loci near the proximal breakpoint reveal distinct imprints of positive selection within the neo-X chromosomal class containing In(4)a. Data from six separate positions examined throughout the proximal region reveal a pattern of recent turnover driven by two independent sweeps among chromosomes with the inverted gene arrangement. Selection-mediated establishment of an extended haplotype associated with recombination-suppressing inversions on the neo-X indicates a pattern of active coadaptation apparently initiated by X-linked transmission and potentially sustained by intralocus sexual conflict.

Figure 1.—

Overview of In(4)a breakpoints isolated in BAC clones of D. americana. (A) Identified cytological positions of breakpoints anchored to scaffolds 12963 and 12723 of the assembled genome sequence of D. virilis. Additional mapped positions used in orienting the scaffolds are listed in supplemental Table S1 (http://www.genetics.org/supplemental/). (B) GBrowse image of annotated genome sequence of D. virilis in regions corresponding to the contents of BAC clones Da_ABa0017N21 and Da_ABa0026O14. Positions of probes dp and raw, which were used to isolate the BAC clones, are indicated by arrowheads connecting with genomic scaffolds. STS markers are annotated in the GBrowse image and delineated by the contents of the two BAC clones. Red lines in each panel identify the positions of the isolated breakpoints.

Figure 2.—

Structure of the sequences at the breakpoints of In(4)a. For each putative ortholog, the gene identification for D. melanogaster is indicated in addition to an asterisk identifying the position of the putative start codon within the sequence of D. americana. Dashed horizontal lines are not drawn to indicated scale. (A) Structure of the sequence in standard arrangement of D. americana, which also corresponds to the genome sequence of D. virilis. Arrowheads indicate the positions of the TE insertion sites. (B) Structure of the sequence in a representative chromosome containing the In(4)a gene arrangement. Crosshatching indicates the orientation of inserted sequences with terminal repeat structures marked with triangles. (C) Folding of the chromosome illustrating sequence identity at the breakpoint regions. Positions of the putative target site duplication (TSD) are consistent with the disruption of a previously intact element. Annotated sequence alignments are available as supplemental material at http://www.genetics.org/supplemental/.

Figure 3.—

Neighbor-joining tree constructed from pairwise estimates of net divergence and rooted with D. virilis. Branch lengths represent net rate of substitution per site estimated from an overall alignment of 6972 nucleotides.

Figure 4.—

Evolutionary model of historical rearrangements, patterns of recombination, and turnover within chromosome 4 of D. americana. Red blocks indicate recombination barriers between arrangements. Green features are putative targets of positive selection and the asterisks indicate a candidate region for feminization. See text for details. (A) Origin of the Fus-In(4)a arrangement through unique recombination event. (B) Recovery of variability on Fus-In(4)a through exchange with parental chromosomes. (C) Origin of In(4)b with hitchhiking. (D) Arrangements of chromosome 4 commonly observed in contemporary populations.