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Invasive Amphibian Gut Microbiota and Functions Shift Differentially in an Expanding Population but Remain Conserved Across Established Populations

  • Environmental Microbiology
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Abstract

Studies of laboratory animals demonstrate extensive variation of host gut microbiomes and their functional capabilities across populations, but how does anthropogenic change impact the microbiomes of non-model species? The anthropogenic movement of species to novel environments can drastically alter animals’ microbiomes; however, factors that shape invasive species gut microbiota during introduction remain relatively unexplored. Through 16S amplicon sequencing on guttural toad (Sclerophrys gutturalis) faecal samples, we determine that residence time does not impact microbiome variation between source and introduced populations. The youngest population (~ 20 years in Cape Town) has the most distinct microbiome and associated functional capabilities, whereas longer residence times (~ 100 years in Réunion and Mauritius) produce less divergent microbial compositional, phylogenetic, and predicted functional diversity and differential abundance from source populations (Durban). Additionally, we show extensive variation of microbial and functional diversity, as well as differential abundance patterns in an expanding introduced population (Cape Town) between core and periphery sites. Contrasting previous studies, we suggest that introduction pathways might be an important factor impacting host microbial divergence. These findings also imply that the microbiome can diverge in accordance with host population dynamics.

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Availability of Data and Material

Raw sequence data will be available in the NCBI Sequence Read Archive (accession number: PRJNA774346).

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Acknowledgements

CW and JM would like to thank Christy Momberg, Erika Nortje, and Suzaan Kritzinger-Klopper for logistical and administrator support. CW and JM thank James Baxter-Gilbert, Julia Riley, Carla Madelaire, Adriana Barsotti, Cláudia Baider, Vincent Florens, Sohan Sauroy-Toucouére, Dominique Strasberg, Damian van Aswegen, and Nitya Mohanty for assistance with field work. Additionally, CW thanks James Baxter-Gilbert and Jan-Hendrik Keet for fruitful discussions during the early stages of this study. CW also thanks Black River Gorges National Park, the Durban Botanical Gardens, and the communities of Notre Dame, Villèle, Pont Payet, and Queensburgh for help collecting toads. CW and JM are grateful to the NCC group for collecting faecal samples in Cape Town. In particular, we would like to thank Jonathan Bell, Lulama Zibi, and Nabeelah Domingo. The Central Analytical Facilities at Stellenbosch University processed and sequenced faecal samples. CW and JM are especially thankful to Alvera and Carel for facilitating the sequencing of samples.

Funding

This study was supported by funding from the DSI-NRF Centre of Excellence for Invasion Biology (CIB) awarded to CW and JM.

Author information

Authors and Affiliations

  1. Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

    Carla Wagener & John Measey

  2. Zoological Research, Foundational Research and Services, South African National Biodiversity Institute, Pretoria, South Africa

    Morne du Plessis

Authors
  1. Carla Wagener
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  2. Morne du Plessis
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Contributions

CW and JM designed the study. CW and JM collected the samples. CW and MDP performed the bioinformatics. CW performed the formal data analyses. CW wrote the manuscript and JM contributed to revisions. All authors have seen and approved the manuscript.

Corresponding author

Correspondence to Carla Wagener.

Ethics declarations

Ethics Approval

Ethical clearance for research was obtained from Stellenbosch University Animal Ethics Committee (Protocol Number ACU-2019–9533). Collections in Cape Town occurred as part of an ongoing eradication programme of Sclerophrys gutturalis to mitigate impacts on the threatened endemic, the western leopard toad Sclerophrys pantherina (Davies et al. 2020), and in Durban and Mauritius under the permission from KZN wildlife (OP 4353/2018) and the Mauritian National Parks and Conservation Services (NP 46/3 V3), respectively.

Conflict of Interest

The authors declare no competing interests.

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Wagener, C., du Plessis, M. & Measey, J. Invasive Amphibian Gut Microbiota and Functions Shift Differentially in an Expanding Population but Remain Conserved Across Established Populations. Microb Ecol 84, 1042–1054 (2022). https://doi.org/10.1007/s00248-021-01896-4

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