Cyprinodon pupfish gut microbiomes

Adaptive radiations offer an excellent opportunity to understand the
eco-evolutionary dynamics of gut microbiota and host niche specialization.
In a laboratory common garden, we compared the gut microbiota of two novel
derived trophic specialist pupfishes, a scale-eater and a molluscivore, to
closely related and distant outgroup generalist populations, spanning both
rapid trophic evolution within 10 kya and stable generalist diets
persisting over 11 Mya. We predicted an adaptive and highly divergent
microbiome composition in the trophic specialists reflecting their rapid
rates of craniofacial and behavioral diversification. We sequenced 16S
rRNA amplicons of gut microbiomes from lab-reared adult pupfishes raised
under identical conditions and fed the same high-protein diet. In contrast
to our predictions, gut microbiota largely reflected phylogenetic distance
among species, rather than generalist or specialist life history, in
support of phylosymbiosis. However, we did find significant enrichment of
Burkholderiaceae bacteria in replicated lab-reared scale-eater
populations. These bacteria sometimes digest collagen, the major component
of fish scales, supporting an adaptive shift. We also found some
enrichment of Rhodobacteraceae and Planctomycetia in lab-reared
molluscivore populations, but these bacteria target cellulose. Overall
phylogenetic conservation of microbiome composition contrasts with
predictions of adaptive radiation theory and observations of rapid
diversification in all other trophic traits in these hosts, including
craniofacial morphology, foraging behavior, aggression, and gene
expression, suggesting that the functional role of these minor shifts in
microbiota will be important for understanding the role of the microbiome
in trophic diversification.

适应性辐射（Adaptive Radiation）为解析肠道菌群与宿主生态位特化的生态-进化动态提供了绝佳研究契机。本研究依托实验室同质园实验，对比了两种新分化出的营养特化型鳉鱼（pupfish）——食鳞鳉（scale-eater）与食软体动物鳉（molluscivore）——的肠道菌群，并以近缘及远缘的外类群广食性种群作为对照；这些类群既涵盖了1万年内快速发生的营养系统演化，也包含了延续超1100万年的稳定广食性食性。我们曾预测，营养特化型类群的肠道菌群组分会呈现适应性且高度分化的特征，以匹配其颅面形态与行为模式的快速分化历程。我们对实验室饲养、处于相同饲养条件且饲喂相同高蛋白日粮的成年鳉鱼的肠道菌群进行了16S rRNA扩增子（16S rRNA amplicon）测序。与我们的预测相悖的是，肠道菌群的组成整体上反映的是物种间的系统发育距离，而非广食性或特化型的生活史，这一结果支持了系统共生（phylosymbiosis）假说。不过，我们确实在重复实验的实验室饲养食鳞鳉种群中，发现了伯克霍尔德氏菌科（Burkholderiaceae）细菌的显著富集。该科细菌部分菌株可消化鱼类鳞片的主要成分——胶原蛋白，这为食鳞习性的适应性演化提供了佐证。我们还在实验室饲养的食软体动物鳉种群中，发现了红杆菌科（Rhodobacteraceae）与浮霉菌纲（Planctomycetia）细菌的一定程度富集，但这类细菌的作用靶点为纤维素。整体而言，肠道菌群组成呈现系统发育保守性，这与适应性辐射理论的预测相悖，也与该类群宿主其余所有营养相关性状的快速分化观测结果形成鲜明对比——这些性状包括颅面形态、觅食行为、攻击性以及基因表达模式。这表明，肠道菌群的这些微小组成变化的功能作用，对于解析菌群在营养系统分化过程中的角色至关重要。