Introduction
Human alterations of animal living environment can adversely affect male fertility through affecting spermatogenesis and sperm quality (Aulsebrook et al., 2020; Kumar & Singh, 2022). On the one hand, due to the close connection between male fertility and population growth, if sperm fail to adapt to the ever-changing environment to buffer the detrimental effects caused by environmental change, a decrease in population fitness and subsequent population collapse will happen (Minnameyer et al., 2021; Walsh et al., 2019). On the other hand, the unique evolutionary feature of spermatozoa, which is they undergo direct and strong selection such as sperm competition and cryptic female choice, make sperm have the capacity to evolve rapidly and provide hopes for adaptation to fast-changing environment (Avidor-Reiss, 2018; Birkhead & Pizzari, 2002; Wang & Gunderson, 2022), and a handful of studies have found sperm traits can evolve in a few generations to adapt to environmental stress (Breckels & Neff, 2014; Vasudeva et al., 2019). However, the genetic mechanisms that enable sperm fast adaptation to environmental degradation are poorly known.
Rapid evolution of sperm requires genetic variation within reproductive genes. Gene duplication has long been regarded as an important force speeding up evolution by facilitating increase in genetic and functional diversities and providing new redundant genetic material (Ames et al., 2010; Conant & Wolfe, 2008; Kondrashov, 2012; Lynch & Katju, 2004). It seems that duplicate genes are potential sources which selection can operate with swiftness and without deleterious effects when environment is undergoing rapid changes. However, when most studies focus on the macroevolutionary pattern in gene duplication, little is known of the fate and importance of duplicate genes in the context of rapid adaptation and evolution of sperm in a short time.
Tree sparrow (Passer montanus ) is an abundant and resident passerine bird in northwest China including Baiyin (BY), a city which is heavily polluted with heavy metals (mainly Cu, Zn, Pb and Cd) resulting from metal mining and smelting (Li et al., 2006; Liu et al., 2016; Nan & Zhao, 2000) for more than 60 years. Sperm traits are known to be sensitive to heavy metal exposure which can result in decreases of sperm count (Akinloye et al., 2006), vability (Chiou et al., 2008; Tabassomi & Alavi-Shoushtari, 2013), motility (Hardneck et al., 2018; Kushawaha et al., 2021) and velocity (Hardneck et al., 2018; Naha & Chowdhury, 2006). Nevertheless, relative to the tree sparrow live in Liujiaxia (LJX), a nearby tourism city selected as a control unpolluted site whose ecological environmental is similar with BY, longer and faster swimming sperm which has been proven to be beneficial for reproductive success have been observed in BY tree sparrow population (Yang et al., 2020a, 2020b). In addition, tree sparrows from the BY population showed significantly higher extra-pair fertilization than LJX population indicating that the sperm competition may be more intense in heavy metal polluted environment (Yang et al., 2021). The unexpected phenotypic variation of sperm and the selective pressures caused by intense sperm competition may indicates that the sperm traits of tree sparrow in BY fast evolved, and this speculation motivates us to explore the molecular basis of sperm phenotype accommodation to the heavy metal pollution through population genomic and transcriptomic. We then identified remarkably duplicate genes are predominant sources driving rapid evolution of sperm in tree sparrow under environmental heavy metal pollution. The results are expected to provide a reference for further exploring the role of duplicate genes in fast adaptation to environmental change and the function of sperm evolution in animal population development under environmental stress.