Dataset Information

Colonization order of bacterial isolates on treefrog embryos impacts microbiome structure in tadpoles.

ABSTRACT: Priority effects, or impacts of colonization order, may have lasting influence on ecological community composition. The embryonic microbiome is subject to stochasticity in colonization order of bacteria. Stochasticity may be especially impactful for embryos developing in bacteria-rich environments, such as the embryos of many amphibians. To determine if priority effects experienced as embryos impacted bacterial community composition in newly hatched tadpoles, we selectively inoculated the embryos of laboratory-raised hourglass treefrogs, Dendropsophus ebraccatus, with bacteria initially isolated from the skin of wild D. ebraccatus adults over 2 days. First, embryos were inoculated with two bacteria in alternating sequences. Next, we evaluated the outcomes of priority effects in an in vitro co-culture assay absent of host factors. We then performed a second embryo experiment, inoculating embryos with one of three bacteria on the first day and a community of five target bacteria on the second. Through 16S rRNA gene amplicon sequencing, we observed relative abundance shifts in tadpole bacteria communities due to priority effects. Our results suggest that the initial bacterial source pools of embryos shape bacterial communities at later life stages; however, the magnitude of those changes is dependent on the host environment and the identity of bacterial colonists.

SUBMITTER: Jones KR

PROVIDER: S-EPMC10031419 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Colonization order of bacterial isolates on treefrog embryos impacts microbiome structure in tadpoles.

Jones Korin Rex KR Hughey Myra C MC Belden Lisa K LK

Proceedings. Biological sciences 20230322 1995

Priority effects, or impacts of colonization order, may have lasting influence on ecological community composition. The embryonic microbiome is subject to stochasticity in colonization order of bacteria. Stochasticity may be especially impactful for embryos developing in bacteria-rich environments, such as the embryos of many amphibians. To determine if priority effects experienced as embryos impacted bacterial community composition in newly hatched tadpoles, we selectively inoculated the embryo ...[more]

PMID: 36946107

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Project description:Climate change is increasing both environmental temperatures and droughts. Many ectotherms respond behaviorally to heat, thereby avoiding damage from extreme temperatures. Within species, thermal tolerance varies with factors such as hydration as well as ontogenetic stage. Many tropical anurans lay terrestrial eggs, relying on environmental moisture for embryonic development. These eggs are vulnerable to dehydration, and embryos of some species can hatch prematurely to escape from drying eggs. Warmer temperatures can accelerate development and thus hatching, but excess heat can kill embryos. Thus, we hypothesize that embryos may show a behavioral thermal tolerance limit, hatching prematurely to avoid potentially lethal warming. If so, because warming and drying are often associated, we hypothesize this limit, measurable as a voluntary thermal maximum, may depend on hydration. We manipulated the hydration of the terrestrial eggs of Agalychnis callidryas, in intact clutches and egg-groups isolated from clutch jelly, then warmed them to assess if embryos hatch early as a behavioral response to high temperatures and whether their thermal tolerance varies with hydration or surrounding structure. We discovered that heating induces hatching; these embryos show a behavioral escape-hatching response that enables them to avoid potentially lethal warming. Hydrated eggs and clutches lost more water and warmed more slowly than dehydrated ones, indicating that hydration buffers embryos from environmental warming via evaporative cooling. Embryos in hydrated clutches tolerated greater warming before hatching and suffered higher mortality, suggesting their behavioral Thermal Safety Margin is small. In contrast, lower thermal tolerance protected dry embryos, and those isolated from clutch jelly, from lethal warming. Heat-induced hatching offers a convenient behavioral assay for the thermal tolerance of terrestrial anuran embryos and the interactive effects of warming and dehydration at an early life stage. This work expands the set of threats against which embryos use hatching in self-defense, creating new opportunities for comparative studies of thermal tolerance as well as integrative studies of self-defense mechanisms at the egg stage.

Project description:Hatching timing is under strong selection and environmentally cued in many species. Embryos use multiple sensory modalities to inform hatching timing and many have spontaneous hatching patterns adaptively synchronized to natural cycles. Embryos can also adaptively shift their hatching timing in response to environmental cues indicating immediate threats or opportunities. Such cued shifts in hatching are widespread among amphibians; however, we know little about what, if anything, regulates their spontaneous hatching. Moreover, in addition to selection on hatching timing, embryos may experience benefits or suffer costs due to the spatial orientation of hatching. Amphibian eggs generally lack internal constraints on hatching direction but embryos might, nonetheless, use external cues to inform hatching orientation. The terrestrial embryos of red-eyed treefrogs, Agalychnis callidryas, hatch rapidly and prematurely in response to vibrational cues in egg-predator attacks and hypoxia if flooded. Here we examined A. callidryas' use of light cues in hatching timing and orientation. To assess patterns of spontaneous hatching and the role of light cues in their diel timing, we recorded hatching times for siblings distributed across three light environments: continuous light, continuous dark, and a 12L:12D photoperiod. Under a natural photoperiod, embryos showed a clear diel pattern of synchronous hatching shortly after nightfall. Hatching was desynchronized in both continuous light and continuous darkness. It was also delayed by continuous light, but not accelerated by continuous dark, suggesting the onset of dark serves as a hatching cue. We examined hatching orientation and light as a potential directional cue for flooded embryos. Embryos flooded in their clutches almost always hatched toward open water, whereas individual eggs flooded in glass cups often failed to do so, suggesting the natural context provides a directional cue. To test if flooded embryos orient hatching toward light, we placed individual eggs in tubes with one end illuminated and the other dark, then flooded them and recorded hatching direction. Most embryos hatched toward the light, suggesting they use light as a directional cue. Our results support that A. callidryas embryos use light cues to inform both when and where to hatch. Both the spatial orientation of hatching and the timing of spontaneous hatching may affect fitness and be informed by cues in a broader range of species than is currently appreciated.

Dataset Information

Colonization order of bacterial isolates on treefrog embryos impacts microbiome structure in tadpoles.

Publications

Colonization order of bacterial isolates on treefrog embryos impacts microbiome structure in tadpoles.

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