Project Summary
Eukaryotic genomes harbor a variety of evolutionarily “selfish” genetic elements (SGEs) that seek to ensure
their transmission at the expense of their hosts. SGEs fall into two broad classes: those that distort fair
Mendelian transmission (e.g., meiotic drive elements) and those that over-replicate relative to the host
genome (e.g., transposable elements, or TEs). TEs have been especially successful, e.g. constituting
~20% of the fruitfly (Drosophila melanogaster) genome, ~45% of the human genome, and ~85% of the
maize genome. Their presence and activity in hosts are major causes of deleterious mutation, genome
instability, and infertility. Eukaryotes have, in response, evolved elaborate surveillance and suppression
mechanisms to detect and mitigate the deleterious effects of TEs, respectively. The resulting conflicts
between TEs and their hosts potentiate molecular evolutionary arms races that can cause rapid population
genetic divergence and speciation— the process by which new species originate. Therefore, understanding
the genetics, molecular biology, and evolution of TE interactions with the host defense apparatus are major
goals of genome biology. Here we propose to investigate the molecular coevolution of two well-studied
retrotransposable elements, R1 and R2, with two closely related fruitfly host species, Drosophila simulans
and D. mauritiana. These fruitfly species are reproductively isolated by multiple genetic incompatibilities
that cause sterility or lethality in their hybrid progeny. We have discovered that one of these genetic
incompatibilities involves the aberrant de-repression of R1 and R2 retrotransposons in somatic tissues and
a syndrome of phenotypic defects— including lethality, delayed egg-to-adult development time, and
disrupted morphological development— characteristic of compromised ribosomal function. Importantly, R1
and R2 insert site-specifically into, and thus disrupt, an appreciable proportion of the linearly arrayed,
multicopy ribosomal genes. While R1 and R2 are normally epigenetically silenced, our preliminary findings
reveal that hybrid genotypes fail to suppress R1 and R2 (but not other TEs), resulting in the expression of
inserted, non-functional ribosomal RNAs. We have therefore identified the species-specific regulation of
two well-characterized TEs that reside in a well-characterized genomic locus, the ribosomal RNA gene
array. The aims of our research project are to combine genetics, molecular biology, cytology, next-
generation sequencing, and evolutionary genomics methods to determine the genes, molecular
mechanisms, and evolutionary forces involved in the coevolution of R1 and R2, with their host species. Our
research promises to shed light on how TEs evolve to evade host surveillance and/or suppression, how
hosts genomes evolve in response, and how the essential, multicopy ribosomal RNA genes are
epigenetically regulated to optimize transcription of TE insertion-free gene copies.
