Department of Biology, Faculty of Sciences, Ghent University, Ghent, Belgium.
Depto. de Biología Animal (Zoología), University of Córdoba, Córdoba, Spain.
BMC Biol. 2024 May 29;22(1):123. doi: 10.1186/s12915-024-01914-0.
Various animal taxa have specialized to living with social hosts. Depending on their level of specialization, these symbiotic animals are characterized by distinct behavioural, chemical, and morphological traits that enable close heterospecific interactions. Despite its functional importance, our understanding of the feeding ecology of animals living with social hosts remains limited. We examined how host specialization of silverfish co-habiting with ants affects several components of their feeding ecology. We combined stable isotope profiling, feeding assays, phylogenetic reconstruction, and microbial community characterization of the Neoasterolepisma silverfish genus and a wider nicoletiid and lepismatid silverfish panel where divergent myrmecophilous lifestyles are observed.
Stable isotope profiling (δC and δN) showed that the isotopic niches of granivorous Messor ants and Messor-specialized Neoasterolepisma exhibit a remarkable overlap within an ant nest. Trophic experiments and gut dissections further supported that these specialized Neoasterolepisma silverfish transitioned to a diet that includes plant seeds. In contrast, the isotopic niches of generalist Neoasterolepisma silverfish and generalist nicoletiid silverfish were clearly different from their ant hosts within the shared nest environment. The impact of the myrmecophilous lifestyle on feeding ecology was also evident in the internal silverfish microbiome. Compared to generalists, Messor-specialists exhibited a higher bacterial density and a higher proportion of heterofermentative lactic acid bacteria. Moreover, the nest environment explained the infection profile (or the 16S rRNA genotypes) of Weissella bacteria in Messor-specialized silverfish and the ant hosts.
Together, we show that social hosts are important determinants for the feeding ecology of symbiotic animals and can induce diet convergence.
各种动物类群已经专门适应与社会宿主一起生活。根据其专业化程度,这些共生动物具有独特的行为、化学和形态特征,能够实现密切的异质种间相互作用。尽管共生动物的共生关系具有重要的功能意义,但我们对与社会宿主共同生活的动物的取食生态学的理解仍然有限。我们研究了银鱼与蚂蚁共生的宿主专业化如何影响其取食生态学的几个组成部分。我们结合稳定同位素分析、取食实验、系统发育重建以及 Neoasterolepisma 属银鱼的微生物群落特征和观察到不同的拟蚁生银鱼类群( Nicoletiidae 和 Lepismatidae )的特征描述,对这一问题进行了研究。
稳定同位素分析(δC 和 δN)表明,杂食性的 Messor 蚂蚁和专门适应蚂蚁的 Neoasterolepisma 的同位素生态位在蚂蚁巢内有显著重叠。取食实验和肠道解剖进一步支持了这些专门适应的 Neoasterolepisma 银鱼向包括植物种子在内的饮食转变。相比之下,一般适应的 Neoasterolepisma 银鱼和一般适应的 Nicoletiidae 银鱼的同位素生态位在共享的巢内环境中与它们的蚂蚁宿主明显不同。拟蚁生的生活方式对取食生态学的影响也体现在内部银鱼微生物组中。与一般适应的物种相比,专门适应 Messor 的物种表现出更高的细菌密度和更高比例的异型发酵乳酸菌。此外,巢内环境解释了 Messor 专门化银鱼和蚂蚁宿主中 Weissella 细菌的感染模式(或 16S rRNA 基因型)。
综上所述,我们表明社会宿主是共生动物取食生态学的重要决定因素,并能诱导取食趋同。