Sex-biased gene expression, sexual antagonism and levels of genetic diversity in the collared flycatcher (Ficedula albicollis) genome

Theoretical work suggests that sexual conflict should promote the maintenance of genetic diversity by the opposing directions of selection on males and females. If such
conflict is pervasive, it could potentially lead to genomic heterogeneity in levels of
genetic diversity an idea that so far has not been empirically tested on a genome-wide
scale. We used large-scale population genomic and transcriptomic data from the
collared flycatcher (Ficedula albicollis) to analyse how sexual conflict, for which we
use sex-biased gene expression as a proxy, relates to genetic variability. Here, we
demonstrate that the extent of sex-biased gene expression of both male-biased and
female-biased genes is significantly correlated with levels of nucleotide diversity in
gene sequences and that this correlation extends to diversity levels also in intergenic
DNA and introns. We find signatures of balancing selection in sex-biased genes but
also note that relaxed purifying selection could potentially explain part of the
observed patterns. The finding of significant genetic differentiation between males
and females for male-biased (and gonad-specific) genes indicates ongoing sexual
conflict and sex-specific viability selection, potentially driven by sexual selection.
Our results thus indicate that sexual antagonism could potentially be considered as
one viable explanation to the long-standing question in evolutionary biology of how
genomes can remain so genetically variable in face of strong natural and sexual
selection.

理论研究表明，性冲突（sexual conflict）可通过雌雄个体间相反的选择方向，促进遗传多样性的维持。若此类性冲突广泛存在，则可能导致遗传多样性水平的基因组异质性——这一观点迄今尚未在全基因组尺度上得到实证检验。我们使用白领姬鹟（collared flycatcher，学名Ficedula albicollis）的大规模群体基因组与转录组数据，以性别偏倚基因表达（sex-biased gene expression）作为性冲突的替代指标，分析性冲突与遗传变异的关联。本研究证实，雄性偏倚与雌性偏倚基因的性别偏倚表达程度，均与基因序列的核苷酸多样性（nucleotide diversity）水平呈显著相关；且这一相关性同样延伸至基因间DNA（intergenic DNA）与内含子（introns）的多样性水平中。我们在性别偏倚基因中发现了平衡选择（balancing selection）的信号，同时也指出，松弛的纯化选择（purifying selection）或许可解释部分观测到的研究结果。雄性与雌性在雄性偏倚（及性腺特异性）基因上存在显著遗传分化的发现，表明正在进行的性冲突与性别特异性生存选择，可能由性选择（sexual selection）驱动。因此，我们的研究结果表明，性拮抗（sexual antagonism）或许可被视为进化生物学中长期存在的核心问题——即面对强烈的自然选择与性选择，基因组如何能维持如此高的遗传多样性——的一个可行解释。