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<p>Abstract</p> <p>Background</p> <p>Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of <it>serpin </it>superfamily genes were subject to massive changes, in contrast to many other genes.</p> <p>Results</p> <p>Here we investigated intron dynamics in the <it>serpin </it>superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate <it>serpin</it>s had been established. In two genes, co-occurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing.</p> <p>Conclusion</p> <p>Multiple intron acquisitions were identified in <it>serpin </it>genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG↑N, previously proposed to serve as intron insertion site. The association of intron gains in the <it>serpin </it>superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.</p>