A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection.
A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection.
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DOI：
10.1371/journal.ppat.1008908
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发表时间：
2020-12
期刊：
影响因子：
6.7
通讯作者：
Catteruccia F
中科院分区：
文献类型：
--
作者：
Marcenac P;Shaw WR;Kakani EG;Mitchell SN;South A;Werling K;Marrogi E;Abernathy DG;Yerbanga RS;Dabiré RK;Diabaté A;Lefèvre T;Catteruccia F
按蚊传播疟原虫已有数百万年的历史，但尚不清楚它们是否承受了感染的适应性成本。本研究报告了冈比亚按蚊和斯蒂芬按蚊这两种重要媒介的处女和交配雌蚊的生殖力不受恶性疟原虫感染的影响，这表明这些人类疟疾寄生虫不会对它们的天然宿主蚊子造成这种繁殖成本。此外，寄生虫的发育不受交配状态的影响。然而，在对不同的恶性疟原虫分离株进行的实地研究中，我们发现交配诱导的促卵因子（MISO）是一种雌性生殖基因，在交配后被类固醇激素20-羟基脱皮激素（20E）的性转移强烈诱导，可以保护雌性免受因感染而产生的繁殖成本。miso沉默的雌性随着感染恶性疟原虫的增加而产生更少的卵，而寄生虫的发育不受这种基因沉默的影响。有趣的是，之前的研究表明，20E的性转移在按蚊属的Cellia物种中特别进化，推动了MISO的共同适应。因此，我们的数据表明，雄性-雌性性互动的进化可能促进了按蚊对细胞亚属恶性疟原虫感染的耐受性，细胞亚属是最重要的疟疾媒介。恶性疟原虫是人类疟疾中最致命的一种，当雌性按蚊叮咬人类并吸食血液以产卵时，它就会传播。迄今为止，人们对感染了恶性疟原虫的按蚊是否会产生适应成本仍知之甚少。本研究发现冈比亚按蚊和斯氏按蚊雌蚊的产卵数量不受恶性疟原虫感染的影响，蚊子的交配状态也不影响疟原虫。然而，在使用布基纳法索献血者的血液用恶性疟原虫感染科鲁兹按蚊（Anopheles coluzzii）的野外实验中，我们发现，干扰一种通常由类固醇激素20-羟基蜕皮激素的性转移触发的基因的表达，会增加卵子发育的成本，因为雌性更容易感染恶性疟原虫，而对寄生虫没有影响。我们的研究结果表明，交配触发的途径可能有助于按蚊预防与恶性疟原虫感染相关的生殖成本，为按蚊在与疟原虫长期存在关联的情况下采取的进化策略提供了新的见解。
Anopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin and mated females of two important vectors—Anopheles gambiae and Anopheles stephensi—is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict this reproductive cost on their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors. Plasmodium falciparum, the deadliest form of human malaria, is transmitted when female Anopheles mosquitoes bite people and take a blood meal in order to develop eggs. To date, it is still poorly understood whether Anopheles mosquitoes that get infected with P. falciparum suffer fitness costs. Here, we find that the number of eggs produced by Anopheles gambiae and Anopheles stephensi females is not affected by P. falciparum infection, and that the mating status of the mosquitoes does not impact the parasite. However, in field experiments infecting a related species, Anopheles coluzzii, with P. falciparum using blood from donors in Burkina Faso, we find that interfering with the expression of a gene normally triggered by the sexual transfer of the steroid hormone 20-hydroxyecdysone induces increasing costs to egg development as females become more infected with P. falciparum, with no impacts on the parasite. The results of our study suggest that pathways triggered by mating may help Anopheles prevent reproductive costs associated with P. falciparum infection, providing new insights into evolutionary strategies adopted by anophelines in the face of a longstanding association with Plasmodium parasites.
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