A neo-sex chromosome that drives postzygotic sex determination in the hessian fly (Mayetiola destructor)

Abstract

Two nonoverlapping autosomal inversions defined unusual neo-sex chromosomes in the Hessian fly (Mayetiola destructor). Like other neo-sex chromosomes, these were normally heterozygous, present only in one sex, and suppressed recombination around a sex-determining master switch. Their unusual properties originated from the anomalous Hessian fly sex determination system in which postzygotic chromosome elimination is used to establish the sex-determining karyotypes. This system permitted the evolution of a master switch (Chromosome maintenance, Cm) that acts maternally. All of the offspring of females that carry Cm-associated neo-sex chromosomes attain a female-determining somatic karyotype and develop as females. Thus, the chromosomes act as maternal effect neo-W's, or W-prime (W') chromosomes, where ZW' females mate with ZZ males to engender female-producing (ZW') and male-producing (ZZ) females in equal numbers. Genetic mapping and physical mapping identified the inversions. Their distribution was determined in nine populations. Experimental matings established the association of the inversions with Cm and measured their recombination suppression. The inversions are the functional equivalent of the sciarid X-prime chromosomes. We speculate that W' chromosomes exist in a variety of species that produce unisexual broods.

Figure 1.—

Chromosome behavior and sex determination in the Hessian fly. (A) Syngamy (1) establishes the germ-line chromosome constitution: ∼32 maternally derived E chromosomes (represented as a single white chromosome) and both maternally derived (black) and paternally derived (gray) autosomes and X chromosomes. During embryogenesis, while the E chromosomes are eliminated, the paternally derived X chromosomes are either retained (2) or excluded (3) from the presumptive somatic cells. When the paternally derived X chromosomes are retained (2), a female-determining karyotype is established. When they are eliminated (3), a male-determining karyotype is established. Thelygenic mothers carry Cm (white arrow), which conditions all of their offspring to retain the X chromosomes. Recombination occurs during oogenesis (4). All ova contain a full complement of E chromosomes and a haploid complement of autosomes and X chromosomes. Chromosome elimination occurs during spermatogenesis (5). Sperm contain only the maternally derived autosomes and X chromosomes. (B) The segregation of Cm (white dot) on a Hessian fly autosome among monogenic families. Thelygenic females produce broods composed of equal numbers of thelygenic (Cm/−) and arrhenogenic (−/−) females (box 1). Arrhenogenic females produce males (box 2). (C) Matings between monogenic and amphigenic families. Cm (white dot) is dominant to the amphigenic-derived chromosomes (gray dot) and generates all-female offspring (box 3). Amphigenic-derived chromosomes are dominant to the arrhenogenic-derived chromosomes (no dot) and generate offspring of both sexes (box 4).

Figure 2.—

Fluorescence in situ hybridization (FISH) revealed A1q inversions. Each panel shows a pair of DAPI-stained A1 polytene chromosomes with the positions of the centromere (arrowhead) and the nucleolus (N) indicated. The hybridization signals associated with the BAC clones that were used as probes are labeled consistently across panels: Mde37d21, green dots; Hf5d5, red dots; CL1c14, blue dots; Hf7b16, red squares. The positions of the more distal inversion, In(A1q1) (1), and the more proximal inversion, In(A1q2) (2), are marked with white lines. (A) A distal shift of Mde37d21 hybridization was diagnostic for In(A1q1) in A1′1/A1 females. (B) Polytene chromosome lacking inversions; bar, 10 μm. (C) A1′2/A1 polytene chromosome pair showing the red fluorescence of BAC Hf7b16 (red squares) at the In(A1q1) breakpoints. (D) A1′2/A1 polytene chromosome pair showing the red fluorescence of the BAC Hf5d5 (red dots) at the In(A1q2) breakpoints. (E and F) Sisters taken from the Israel population were segregating as In(A1q1) heterozygotes (E) and non-In(A1q1) homozygotes (F).

Figure 3.—

FISH-based map of BAC-based contigs along Hessian fly chromosome A1. The chromosome is diagramed as a shaded vertical line and the positions of the centromere (constriction) and nucleolus (N) are indicated. Horizontal lines indicate the relative positions of each of 74 numbered contigs. The number of BACs in each contig and the BACs used as probes to position the contig on the chromosome are indicated. BACs from the CL library are preceded by the designation “CL.” All other BACs are from the Hf library. A dash between the two clones used as probe indicates that it was possible to order their positions on the chromosome; the first clone listed was most proximal. A comma between the BACs indicates that the orientation of the contig could not be determined. In(A1q1) (arrow 1) and In(A1q2) (arrow 2) were identified on the long arm of chromosome A1. The order and orientation of the contigs within the inversions were the reverse of those shown on the map.

Figure 4.—

A1 chromosomes inherited from an exceptional male. DAPI-stained polytene chromosomes show the green hybridization signal of BAC Mde37d21 (green dots) and the red hybridization signal of BAC Hf5d5 (red dots). All images are shown at the same magnification. (A) Matings between the exceptional male and an arrhenogenic female produced male offspring with A1 polytene chromosomes heterozygous for chromosomes A1′2 and A1. (B and C) Matings between the same exceptional male and a thelygenic female produced female offspring that were either heterozygous A1′2/A1 (B) or homozygous A1′2 (C). Bar (horizontal white bar), 10 μm.

Figure 5.—

A1 chromosome inversions influence A1q recombination. (A) The relative physical positions of five DNA markers and In(A1q1) (arrow 1) and In(A1q2) (arrow 2) are shown next to a Giemsa-stained polytene chromosome lacking the inversions. The positions of the centromere (arrowhead) and the nucleolus (N) are indicated. To the right of the chromosome are maps B, C, and D showing the relative genetic positions of the same markers and the Cm locus (where possible). Mapping populations consisted of the offspring of (B) an arrhenogenic female (A1/A1; n = 54), (C) a thelygenic female heterozygous for In(A1q1) (A1′1/A1; n = 50), and (D) a thelygenic female heterozygous for both In(A1q1) and In(A1q2) (A1′2/A1; n = 132). Genetic distances (cM ± SE) between markers are indicated to the right of each map. Genetic distances that are significantly different between maps are indicated by the letters “a,” differences between maps A and B; “b,” differences between maps A and C; and “c,” differences between maps B and C (chi-square two-way test, P < 0.01).