Grizard Stéphanie, Versteegh Maaike A, Ndithia Henry K, Salles Joana F, Tieleman B Irene
Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands; Department of Microbial Ecology, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands.
Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands.
PLoS One. 2015 Apr 16;10(4):e0121716. doi: 10.1371/journal.pone.0121716. eCollection 2015.
Microbial invasion of egg contents is a cause of embryonic death. To counter infection risks, the embryo is protected physically by the eggshell and chemically by antimicrobial proteins. If microbial pressure drives embryo mortality, then females may have evolved, through natural selection, to adapt their immune investment into eggs. Although frequently hypothesized, this match between immune allocation and microorganisms has not been explored yet. To examine if correlations between microbes on eggs and immunity in eggs exist, we collected eggs from red-capped larks (Calandrella cinerea) and simultaneously examined their bacterial communities and antimicrobial components--pH, lysozyme and ovotransferrin--during natural incubation. Using molecular techniques, we find that bacterial communities are highly dynamic: bacterial abundance increases from the onset to late incubation, Shannon's α-diversity index increases during early incubation stages, and β-diversity analysis shows that communities from 1 day-old clutches are phylogenetically more similar to each other than the older ones. Regarding the antimicrobials, we notice a decrease of pH and lysozyme concentration, while ovotransferrin concentration increases during incubation. Interestingly, we show that two eggs of the same clutch share equivalent immune protection, independent of clutch age. Lastly, our results provide limited evidence of significant correlation between antimicrobial compounds and bacterial communities. Our study examined simultaneously, for the first time in a wild bird, the dynamics of bacterial communities present on eggshells and of albumen-associated antimicrobial components during incubation and investigated their relationship. However, the link between microorganisms and immunity of eggs remains to be elucidated further. Identifying invading microbes and their roles in embryo mortality, as well as understanding the role of the eggshell microbiome, might be key to better understand avian strategies of immune maternal investment.
微生物侵入卵内容物是胚胎死亡的一个原因。为了应对感染风险，胚胎在物理上受到蛋壳的保护，在化学上受到抗菌蛋白的保护。如果微生物压力导致胚胎死亡，那么雌性可能通过自然选择进化出调整其对卵的免疫投入的能力。尽管这一假设经常被提出，但免疫分配与微生物之间的这种匹配关系尚未得到研究。为了检验卵上的微生物与卵内免疫之间是否存在相关性，我们从红顶云雀（Calandrella cinerea）收集了卵，并在自然孵化期间同时检测了它们的细菌群落和抗菌成分——pH值、溶菌酶和卵转铁蛋白。使用分子技术，我们发现细菌群落具有高度动态性：细菌丰度从孵化开始到后期增加，香农α多样性指数在孵化早期阶段增加，β多样性分析表明，1日龄窝卵的群落彼此之间在系统发育上比年龄较大的群落更相似。关于抗菌物质，我们注意到pH值和溶菌酶浓度降低，而卵转铁蛋白浓度在孵化期间增加。有趣的是，我们发现同一窝的两个卵具有同等的免疫保护，与窝卵年龄无关。最后，我们的结果提供了有限的证据表明抗菌化合物与细菌群落之间存在显著相关性。我们的研究首次在野生鸟类中同时检测了孵化期间蛋壳上存在的细菌群落和与蛋白相关的抗菌成分的动态变化，并研究了它们之间的关系。然而，微生物与卵免疫之间的联系仍有待进一步阐明。识别入侵微生物及其在胚胎死亡中的作用，以及了解蛋壳微生物群的作用，可能是更好地理解鸟类母体免疫投资策略的关键。
