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We describe here the  Drosophila  gene  hydra  that appears to have originated de novo in the  melanogaster  subgroup and subsequently evolved in both structure and expression level in  Drosophila melanogaster  and its sibling species.  D. melanogaster hydra  encodes a predicted protein of ~300 amino acids with no apparent similarity to any previously known proteins. The syntenic region flanking  hydra  on both sides is found in both  D. ananassae  and  D. pseudoobscura,  but  hydra  is found only in  melanogaster  subgroup species, suggesting that it originated less than ~13 million y ago. Exon 1 of  hydra  has undergone recurrent duplications, leading to the formation of nine tandem alternative exon 1s in  D. melanogaster.  Seven of these alternative exons are flanked on their 3′ side by the transposon  DINE-1  ( Drosophila  interspersed element-1). We demonstrate that at least four of the nine duplicated exon 1s can function as alternative transcription start sites. The entire  hydra  locus has also duplicated in  D. simulans  and  D. sechellia .  D. melanogaster hydra  is expressed most intensely in the proximal testis, suggesting a role in late-stage spermatogenesis. The coding region of  hydra  has a relatively high Ka/Ks ratio between species, but the ratio is less than 1 in all comparisons, suggesting that  hydra  is subject to functional constraint. Analysis of sequence polymorphism and divergence of  hydra  shows that it has evolved under positive selection in the lineage leading to  D. melanogaster.  The dramatic structural changes surrounding the first exons do not affect the tissue specificity of gene expression:  hydra  is expressed predominantly in the testes in  D. melanogaster, D. simulans,  and  D. yakuba.  However, we have found that expression level changed dramatically (~ >20-fold) between  D. melanogaster  and  D. simulans.  While  hydra  initially evolved in the absence of nearby transposable element insertions, we suggest that the subsequent accumulation of repetitive sequences in the  hydra  region may have contributed to structural and expression-level evolution by inducing rearrangements and causing local heterochromatinization. Our analysis further shows that recurrent evolution of both gene structure and expression level may be characteristics of newly evolved genes. We also suggest that late-stage spermatogenesis is the functional target for newly evolved and rapidly evolving male-specific genes.

Evolution of hydra, a Recently Evolved Testis-Expressed Gene with Nine Alternative First Exons in Drosophila melanogaster