Sperm competitive advantage of a rare mitochondrial haplogroup linked to differential expression of mitochondrial oxidative phosphorylation genes
Sperm competitive advantage of a rare mitochondrial haplogroup linked to differential expression of mitochondrial oxidative phosphorylation genes
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DOI：
10.1111/jeb.13536
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发表时间：
2019-09
影响因子：
2.1
通讯作者：
J. A. Zeh;Maya A Zawlodzki;Melvin M. Bonilla;Eleanor Su-Keene;Michael V. Padua;D. W. Zeh
中科院分区：
文献类型：
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作者：
J. A. Zeh;Maya A Zawlodzki;Melvin M. Bonilla;Eleanor Su-Keene;Michael V. Padua;D. W. Zeh
线粒体的母系遗传创造了一个性别特异性的选择性筛选，通过该筛选，对男性有害而对女性有害的线粒体突变积累起来，并导致寿命和疾病易感性的性别差异。由于卵子和精子处于破坏性选择之下，精子被预测特别容易受到母体遗传产生的遗传负荷的影响，但线粒体参与男性生育的证据有限且有争议。在这里，我们利用共存的两个不同的线粒体单倍型群（A和B2）在新热带区蛛形纲动物的线粒体在精子竞争中的作用进行调查。DNA分析表明，在精子竞争实验中，携带B2的雄性比A雄性产生的后代多三倍以上，这种B2竞争优势不能用雌性线粒体单倍群或雄性核遗传背景来解释。睾丸组织的RNA-Seq表明线粒体氧化磷酸化（OXPHOS）基因在B2竞争优势中的差异表达，包括B2男性中atp 8的22倍上调。先前的比较基因组分析揭示了差异表达基因中功能显著的氨基酸替换，表明线粒体单倍型组不仅在表达上不同，而且在DNA序列和蛋白质功能上也不同。然而，线粒体单倍型类群对精子数量或精子活力没有影响，并且，当雌性与单个雄性交配时，雄性单倍型类群、雌性单倍型类群以及雄性/雌性单倍型类群之间的相互作用都不显著影响雌性生殖成功。因此，我们的研究结果表明，线粒体对男性生殖的影响在非竞争性环境中可能经常未被发现，并且可能在自然界中比目前所认识的更重要。
Maternal inheritance of mitochondria creates a sex‐specific selective sieve through which mitochondrial mutations harmful to males but not females accumulate and contribute to sexual differences in longevity and disease susceptibility. Because eggs and sperm are under disruptive selection, sperm are predicted to be particularly vulnerable to the genetic load generated by maternal inheritance, yet evidence for mitochondrial involvement in male fertility is limited and controversial. Here, we exploit the coexistence of two divergent mitochondrial haplogroups (A and B2) in a Neotropical arachnid to investigate the role of mitochondria in sperm competition. DNA profiling demonstrated that B2‐carrying males sired more than three times as many offspring in sperm competition experiments than A males, and this B2 competitive advantage cannot be explained by female mitochondrial haplogroup or male nuclear genetic background. RNA‐Seq of testicular tissues implicates differential expression of mitochondrial oxidative phosphorylation (OXPHOS) genes in the B2 competitive advantage, including a 22‐fold upregulation of atp8 in B2 males. Previous comparative genomic analyses have revealed functionally significant amino acid substitutions in differentially expressed genes, indicating that the mitochondrial haplogroups differ not only in expression but also in DNA sequence and protein functioning. However, mitochondrial haplogroup had no effect on sperm number or sperm viability, and, when females were mated to a single male, neither male haplogroup, female haplogroup nor the interaction between male/female haplogroup significantly affected female reproductive success. Our findings therefore suggest that mitochondrial effects on male reproduction may often go undetected in noncompetitive contexts and may prove more important in nature than is currently appreciated.