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.