Hybrid larval lethality of Drosophila is caused by parent-of-origin expression: an insight from imaginal discs morphogenesis of Lhr pausing rescue hybrids of D. melanogaster and D. simulans

Abstract

Hybrid males that inherit haploid set of chromosomes along with Hybrid male rescue, (Hmr+) gene from D. melanogaster mother and an autosomal set with Lethal hybrid rescue, (Lhr+) gene from D. simulans father, die at the larval/pupal transition phase due to insufficient growth of imaginal disc tissues. Comparable pattern reminiscent of hybrid F1female lethality was noted when D. melanogaster compound females were crossed with D. simulans males. The lethality is suppressed when the hybrids inherit one mutant allele of hybrid incompatibility gene (either Lhr−, or Hmr−) from either of the parent. In order to better understand the cause of lethality of F1 hybrids at larval stage, the imaginal discs development of lethal hybrids were examined and compared with those of ‘rescued’ hybrids with Lhr− and parental species. The study revealed the following major findings: (a) when hybrid male and female larvae carry only D. melanogaster X chromosome(s) in presence of both Lhr+ and Hmr+ genes, broad-ranging cell death reaction was induced in the disc tissues and eventually death of the hybrid larvae, (b) when hybrid females carry the X chromosome of both species in the background of maternal cytoplasm of D. melanogaster, the frequency of cell death in the discs was reduced significantly and discs were able to metamorphose, (c) when hybrid males and females inherit one set of autosome from Lhr null strain of D. simulans, the frequency of non-apoptotic cell death in the discs was suppressed significantly and discs development were restored, although the discs displayed fluctuating asymmetric of development. To understand the defects in the chromosomal organization associated with abnormal development of the ‘rescued’ hybrids, the functional organization of the polytene chromosomes of the ‘rescued’ hybrids were examined. It was noted that incomplete pairing of the autosomes of two species along with abnormal X chromosomal telomeric structure may have some bearing on developmental defects of the ‘rescued’ hybrids. From the results it is suggested that (1) cell death reaction in the imaginal discs of the larval lethal hybrids may be the result of divergent lineage of maternal and paternal sets of chromosomes in zygote in presences of two species specific mediator genes, Lhr+, and Hmr+, (2) suppression of larval lethality, in absence of Lhr function, indicated that the non-apoptotic type of cell death factor in the disc cells was controlled genetically by the two mediator genes in the disc cells, (3) re-specification of compartmental organization of paternal segment polarity genes in ‘rescued’ hybrid discs might cause non-random tissue damages and eventually the apoptotic type of cell death resulting into asymmetric development of the appendages in hybrids. In sum, our data revealed that cell death reaction in imaginal discs, associated with larval lethality in hybrids was a developmentally controlled program, through incompatible interactions between species specific mediator genes, Lhr+, Hmr+ and D. melanogaster X chromosome and the pattern of cell death reaction in the discs was different from apoptosis.