The creation of new genes is a major force of evolution. Despite as an important mechanism that generated new genes, segmental duplication (SD) has yet to be accurately identified and fully characterized in birds because the repetitive complexity leads to misassignment and misassembly of sequence. In addition, SD may lead to new gene copies, which makes it possible to test the “out of testis” hypothesis which suggests genes are frequently born with testis-specific expression. Using a high-quality chromosome-level assembly, we performed a systematic analysis and presented a comprehensive landscape of SDs in tree sparrow (Passer montanus). We detected co-localization of newly expanded genes and long terminal repeat retrotransposons (LTR-RTs), both of which are derived from SDs and enriched in microchromosomes. The newly expanded genes are mostly found in eight families including C2H2ZNF, OR, PIM, PAK, MROH, HYDIN, HSF and ITPRIPL. The large majority of new members of these eight families have evolved to pseudogenes, whereas there still some new copies preserved transcriptional activity. Among the transcriptionally active new members, new genes from different families with diverse structures and functions shared a similar testis-biased expression pattern, which is consistent with the “out of testis” hypothesis. Through a case analysis of the high-quality genome assembly of tree sparrow, we reveal that the SDs contribute to the formation of new genes. Our study provides a comprehensive understanding of the emergence, expression and fate of duplicated genes and how the SDs might participate in these processes and shape genome evolution.

Environmental pollution can result in poor sperm quality either directly or indirectly. However, adaptive and compensatory sperm morphology change and motility improvement rapidly evolved in tree sparrow (Passer montanus) inhabited the polluted area within the past 65 years. To identify the genetic underpinnings of the rapidly evolved sperm phenotype, both the population genomic and transcriptomic methods were used in our study. We identified a gene encoding serine/threonine protein kinase PIM1 which may drive the rapid phenotypic evolution of sperm. An unprecedent and remarkably expansion of PIM gene family caused by tandem and segmental duplication of PIM1 was subsequently noticed in tree sparrow genome. Most of the PIM1 duplicates showed a testis-specific expression pattern, suggesting their functions related to male reproduction. Furthermore, the elevated expression level of PIM1 was consistent with our earlier findings of longer and faster swimming sperm in polluted site, indicating an important role of duplicated PIM1 in facilitating rapid evolution of sperm. Our results suggested that the duplicated PIM1 provide sources of genetic variation that enable rapid evolution of sperm under environmental heavy metal pollution. The findings in this study verified the duplicated genes can be targets of selection and predominant sources for rapid adaptation to environmental change and shed lights on the sperm evolution under environmental stress.