Academic journal article Genetics

Developmental and Cell Cycle Progression Defects in Drosophila Hybrid Males

Academic journal article Genetics

Developmental and Cell Cycle Progression Defects in Drosophila Hybrid Males

Article excerpt

ABSTRACT

Matings between D. melanogaster females and males of sibling species in the D. melanogaster complex yield hybrid males that die prior to pupal differentiation. We have reexamined a previous report suggesting that the developmental defects in these lethal hybrid males reflect a failure in cell proliferation that may be the consequence of problems in mitotic chromosome condensation. We also observed a failure in cell proliferation, but find in contrast that the frequencies of mitotic figures and of nuclei staining for the mitotic marker phosphohistone H3 in the brains of hybrid male larvae are extremely low. We also found that very few of these brain cells in male hybrids are in S phase, as determined by BrdU incorporation. These data suggest that cells in hybrid males are arrested in either the G^sub 1^ or G^sub 2^ phases of the cell cycle. The cells in hybrid male brains appear to be particularly sensitive to environmental stress; our results indicate that certain in vitro incubation conditions induce widespread cellular necrosis in these brains, causing an abnormal nuclear morphology noted by previous investigators. We also document that hybrid larvae develop very slowly, particularly during the second larval instar. Finally, we found that the frequency of mitotic figures in hybrid male larvae mutant for Hybrid male rescue (Hmr) is increased relative to lethal hybrid males, although not to wild-type levels, and that chromosome morphology in Hmr^sup -^ hybrid males is also not completely normal.

SPECIATION requires reproductive isolation between diverging populations (Mayr 1942). One type of barrier that can isolate emerging species is the inviability or infertility of hybrids. For example, although the species in the Drosophila melanogaster complex (D. melanogaster and its sibling species D. simulans, D. mauritiana, and D. sechellia) are closely related and morphologically almost indistinguishable, matings between D. melanogaster females and males of any of the sibling species yield F1 females that are semiviable but sterile, as well as males that die as developmentally delayed larvae or pseudopupae with small or nonexistent imaginal discs (Sturtevant 1920, 1929; Hadorn 1961; Sánchez and Dübendorfer 1983).

The lethality of hybrid males appears to be due to an incompatibility between one or more genes on the D. melanogaster X chromosome and one or more autosomal genes in the other species (Sturtevant 1920, 1929; Pontecorvo 1943; Hadorn 1961; Hutter et al. 1990; Yamamoto 1992; Brideau et al. 2006). Hybrid lethality is not sex specific, since hybrid females homozygous for the D. melanogaster X chromosome also die at the same stage of development (Hutter et al. 1990; Orr 1993). The X-linked Hybrid male rescue (Hmr) gene in D. melanogaster and the autosomal Lethal hybrid rescue (Lhr) gene in D. simulans are major players in causing this hybrid lethality because loss-of-function alleles in these genes suppress the lethality (Watanabe 1979; Hutter and Ashburner 1987; Barbash et al. 2000, 2003; Brideau et al. 2006). Despite this progress in studying the genetic basis of hybrid male inviability, the developmental causes of the phenomenon remain poorly understood. One study found that hybrid males suffer from limited cell proliferation and proposed that this phenotype is due to a failure in mitotic chromosome condensation (Orr et al. 1997). These authors observed that uncultured brain cells have a very low frequency of normally condensed metaphase chromosomes and also found that hybrid females produce only small abdominal clones of D. melanogaster X chromosome tissue. The investigators further found that the brains of hybrid male larvae incubated in 0.7% NaCl and in both the presence and the absence of colchicine (a drug used to arrest cells in metaphase) contained very few normal mitotic figures, but many cells displayed masses of diffuse chromatin. These latter cells were interpreted to have entered a defective mitosis in which the chromatin remains undercondensed relative to that normally seen in the prometaphase/metaphase mitotic figures in neuroblasts from each pure species. …

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