Commensal microbiota and host metabolic divergence are associated with the adaptation of Diploderma vela to spatially heterogeneous environments

Abstract

Heterogeneous environment adaptation is critical to understand the species evolution and response to climate change. However, how narrow-range species adapt to micro-geographic heterogeneity has been overlooked, and there is a lack of insights from metabolism and commensal microbiota. Here, we studied the environmental adaptation for 3 geographic populations (>40 km apart) of Diploderma vela, a lizard endemic to dry-hot valleys of the Hengduan Mountain Region. The climatic boundary caused a cooler, droughtier, and barren environment for northernmost population (RM) than the middle (QZK) and southernmost populations (FS). Correspondingly, significant divergences in liver and muscle metabolism and commensal microbiota were detected between RM and QZK or FS individuals, but not between QZK and FS individuals. Phospholipid composition, coenzyme level (i.e. pyridoxal and NAD + ), and cholesterol metabolism (e.g. androgen and estriol synthesis) constituted the major metabolic difference between RM and QZK/FS groups. FS and QZK individuals kept abundant Proteobacteria and antifungal strains, while RM individuals maintained more Firmicutes and Bacteroidota. Strong associations existed between varied host metabolite and gut microbes. How were these interpopulation variations associated to the environment adaptation were discussed. These results provided some novel insights into the environmental adaptation and implicated the consequence of climate change on narrow-range species.

Multi-Omics Approaches Revealed the Associations of Host Metabolism and Gut Microbiome With Phylogeny and Environmental Adaptation in Mountain Dragons

“…1 This information is detailed in Supplementary Table 1 . The gut microbiome and tissue metabolomics data of D. vela have been published previously ( Zhu et al, 2021c ).…”

“…Extracted supernatants were analyzed by LC (1,290 Infinity LC, Agilent) coupled with quadrupole-time-of-flight mass spectrometry (Triple TOF 5,600 +, AB SCIEX). The details in the metabolic profiling followed the methods described by Zhu et al (2021c) . Metabolite data were processed using XCMS software 2 and Microsoft Excel (Microsoft, Redmond, WA, United States).…”

“…Environmental heterogeneity can drive adaptive divergences between populations at both genetic and physiological levels ( Rainey and Travisano, 1998 ; Valladares et al, 2014 ). These interpopulation variations play a fundamental role in maintaining a species’ genetic or functional diversity and response to climate change ( Charmantier et al, 2008 ; Zhu et al, 2021c ). Moreover, adaptive genetic divergence may result in ecological speciation if it causes some form of reproductive isolation ( Schluter, 2000 ; Rundle and Nosil, 2005 ).…”

“…Currently, the formation of Diploderma diversity in HMR has not been studied systematically, and vicariant isolation, ecological divergence, and the low migration capacity of lizards (within 10 km; Southwood and Avens, 2010 ) are all potential drivers. The distribution areas of the Diploderma species are narrow but highly heterogeneous in terms of spatial climatic factors ( Zhu et al, 2021c ). This makes the Diploderma species an ideal model for investigating environmental adaptation at a micro-geographic scale.…”

Intestinal microbiota in various animals

“…In this spirit, Integrative Zoology publishes one more special subsection in this issue. Zhu et al (2022) revealed that the adaptation of animal gut microbiota and metabolic characters to spatial heterogeneous environments could provide mechanistic insights into the evolution and enable reliable prediction on population distribution with climate change. This multi-omics study found that Diploderma vela populations with different climatic background showed significant divergence in their muscle and liver metabolome and gut commensal microbiota, and this was not observed between populations that shared similar climatic factors despite of comparable geographical distance.…”