Temperature and the microbial environment alter brain morphology in a larval amphibian

Abstract

Understanding how the global climate impacts the physiology of wildlife animals is of importance. Amphibians are particularly sensitive to climate change, and it is hypothesized that rising temperatures impair their neurodevelopment. Temperature influences the composition of the gut microbiota, which is critical to host neurodevelopment through the microbiota-gut-brain (MGB) axis. Most research investigating the link between the gut microbiota and neurodevelopment occurs in germ-free mammalian model systems, leaving the nature of the MGB axis in non-mammalian wildlife unclear. Here, we tested the hypothesis that the temperature and the microbial environment in which tadpoles were raised shapes neurodevelopment, possibly through the MGB axis. Newly hatched Green Frog tadpoles (Lithobates clamitans) were raised in natural pond water or autoclaved pond water, serving as an experimental manipulation of the microbiota by reducing colonizing microbes, at three different water temperatures: 14°C, 22°C, and 28°C. Neurodevelopment was analyzed through measures of relative brain mass and morphology of brain structures of interest. We found that tadpole development in warmer temperatures increased relative brain mass and optic tectum width and length. Further, tadpole development in autoclaved pond water increased relative optic tectum width and length. Additionally, the interaction of treatments altered relative diencephalon length. Lastly, we found that variation in brain morphology was associated with gut microbial diversity and the relative abundance of individual bacterial taxa. Our results indicate that both environmental temperature and microbial communities influence relative brain mass and shape. Furthermore, we provide some of the first evidence for the MGB axis in amphibians.

Environmental bacteria increase population growth of hydra at low temperature

“…Environmental microbiota is considered important for animal health because of its contribution to proper immune maturation in animals possessing an adaptive immune system. While research in vertebrates has unveiled numerous instances where the presence of environmental microbes can positively affect animal health ( Knutie et al, 2017 ; Fontaine et al, 2022 ; Emerson et al, 2023 ), less is understood about their role and potential fitness consequences in invertebrates that lack an adaptive immune system.…”

“…Studies done on frogs, for instance, have shown that raising tadpoles in an environment with reduced microbial diversity (autoclaved lake water) disrupts their gut microbiota and affects subsequent resistance to parasitic nematode infections, likely through affecting immune maturation ( Knutie et al, 2017 ). Likewise, raising tadpoles in water with reduced microbial diversity exhibited altered brain morphology ( Emerson et al, 2023 ) and reduced stress tolerance under both high and low temperature stress, which ultimately impacted their fitness ( Fontaine et al, 2022 ). All these examples resonate with the “Hygiene Hypothesis” and the recently proposed One Health principle, which posit that aspects of the wider environment are closely linked to the health of humans and animals ( Yazdanbakhsh et al, 2002 ; Trinh et al, 2018 ).…”

The Circadian Rhythm of the Behavior and Gut Microbiota in Dybowski’s Frogs (Rana dybowskii) during the Autumn Migration Period

“…In Rana sphenocephala , the gut microbiota of tadpoles is influenced by diet composition [ 24 ]. In green frog ( Lithobates clamitans ) tadpoles, both environmental temperature and microbial communities influence relative brain mass and shape [ 25 ]. Research on Asiatic toads ( Bufo gargarizans ) has revealed considerable structural differences between the large and small intestines [ 26 ].…”