Linking pathogen–microbiome–host interactions to explain amphibian population dynamics

Torres‐Sánchez, María; Longo, Ana V.

doi:10.1111/mec.16701

Cited by 12 publications

(12 citation statements)

References 104 publications

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“…There is mixed evidence in the literature of the effects of Bd on genetic diversity, with some studies showing lower genetic diversity in frog populations impacted by Bd (e.g. Byrne et al., 2021; Torres‐Sánchez & Longo, 2022), while others showed stable or even increased genetic diversity in frog populations infected with Bd (e.g. Banks et al., 2020; Horner et al., 2017) including in a microsatellite study of boreal toads from Glacier National Park in Montana (Addis et al., 2015).…”

Section: Discussionmentioning

confidence: 99%

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Trumbo,

Hardy,

Crockett

et al. 2023

Molecular Ecology

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Wildlife diseases are a major global threat to biodiversity. Boreal toads (Anaxyrus [Bufo] boreas) are a state‐endangered species in the southern Rocky Mountains of Colorado and New Mexico, and a species of concern in Wyoming, largely due to lethal skin infections caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). We performed conservation and landscape genomic analyses using single nucleotide polymorphisms from double‐digest, restriction site‐associated DNA sequencing in combination with the development of the first boreal toad (and first North American toad) reference genome to investigate population structure, genomic diversity, landscape connectivity and adaptive divergence. Genomic diversity (π = 0.00034–0.00040) and effective population sizes (Ne = 8.9–38.4) were low, likely due to post‐Pleistocene founder effects and Bd‐related population crashes over the last three decades. Population structure was also low, likely due to formerly high connectivity among a higher density of geographically proximate populations. Boreal toad gene flow was facilitated by low precipitation, cold minimum temperatures, less tree canopy, low heat load and less urbanization. We found >8X more putatively adaptive loci related to Bd intensity than to all other environmental factors combined, and evidence for genes under selection related to immune response, heart development and regulation and skin function. These data suggest boreal toads in habitats with Bd have experienced stronger selection pressure from disease than from other, broad‐scale environmental variations. These findings can be used by managers to conserve and recover the species through actions including reintroduction and supplementation of populations that have declined due to Bd.

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Section: Discussionmentioning

confidence: 99%

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Trumbo,

Hardy,

Crockett

et al. 2023

Molecular Ecology

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“…Habitat split-related reductions in immunogenetic diversity and changes in MHC class II genotype abundance and expression within populations could covary with microbiome structure and function, as observed in fragmented populations of Ozark hellbenders Cryptobranchus alleganiensis bishopi (Hern andez-G omez, Briggler & Williams, 2018); see also Grieves et al (2021) for a similar correlation between pairwise MHC similarity and preen gland microbiota in birds. Torres-S anchez & Longo (2022) found heterozygote advantage to recruitment of beneficial symbionts, providing defences that increase host fitness. Likewise, microbiome recruitment and natural selection and/or sustained glucocorticoid elevation during development in poor aquatic habitat within a disturbed landscape matrix could affect the development of juvenile skin defences (Hayes, 1995;Knutie et al, 2017b).…”

Section: Potential Mechanisms Linking Habitat Split and Elements Of A...mentioning

confidence: 99%

“…(2021) for a similar correlation between pairwise MHC similarity and preen gland microbiota in birds. Torres‐Sánchez & Longo (2022) found heterozygote advantage to recruitment of beneficial symbionts, providing defences that increase host fitness. Likewise, microbiome recruitment and natural selection and/or sustained glucocorticoid elevation during development in poor aquatic habitat within a disturbed landscape matrix could affect the development of juvenile skin defences (Hayes, 1995; Knutie et al ., 2017 b ).…”

Section: Potential Mechanisms Linking Habitat Split and Elements Of A...mentioning

confidence: 99%

Habitat split as a driver of disease in amphibians

et al. 2023

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Anthropogenic habitat disturbance is fundamentally altering patterns of disease transmission and immunity across the vertebrate tree of life. Most studies linking anthropogenic habitat change and disease focus on habitat loss and fragmentation, but these processes often lead to a third process that is equally important: habitat split. Defined as spatial separation between the multiple classes of natural habitat that many vertebrate species require to complete their life cycles, habitat split has been linked to population declines in vertebrates, e.g. amphibians breeding in lowland aquatic habitats and overwintering in fragments of upland terrestrial vegetation. Here, we link habitat split to enhanced disease risk in amphibians (i) by reviewing the biotic and abiotic forces shaping elements of immunity and (ii) through a spatially oriented field study focused on tropical frogs. We propose a framework to investigate mechanisms by which habitat split influences disease risk in amphibians, focusing on three broad host factors linked to immunity: (i) composition of symbiotic microbial communities, (ii) immunogenetic variation, and (iii) stress hormone levels. Our review highlights the potential for habitat split to contribute to host‐associated microbiome dysbiosis, reductions in immunogenetic repertoire, and chronic stress, that often facilitate pathogenic infections and disease in amphibians and other classes of vertebrates. We highlight that targeted habitat‐restoration strategies aiming to connect multiple classes of natural habitats (e.g. terrestrial–freshwater, terrestrial–marine, marine–freshwater) could enhance priming of the vertebrate immune system through repeated low‐load exposure to enzootic pathogens and reduced stress‐induced immunosuppression.

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“…Previous studies have shown that genetic distribution of MHC class II alleles was strongly influenced by evolutionary processes such as migration, drift, selection, and demography in amphibians (Cortázar-Chinarro et al, 2017;Luquet et al, 2019). However, very little is known about how evolutionary processes influence skin microbiota diversity in amphibians (Belasen et al, 2021;Torres Sánchez & Longo, 2022). Despite that our results suggested a similar pattern of alpha diversity between regions and populations, the relative abundance of shared ASVs, beta diversity and, thereby, the bacterial community structure composition varied between regions and populations.…”

Section: Microbiome Variation Between Regions and Populationsmentioning

confidence: 99%

“…Among these diseases, chytridiomycosis stands out as an emerging disease caused by the chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) inflicting amphibian mass die-offs worldwide (Kilpatrick, Briggs, & Daszak, 2010;Martel et al, 2014;Scheele et al, 2019). Recent studies demonstrate the importance of the skin microbiota in amphibian innate immune defense against Bd (Bates et al, 2018;Rebollar et al, 2016;Torres Sánchez & Longo, 2022). Hence, investigating how host MHC genetics, environment and evolutionary history determine the skin microbial diversity and composition of amphibian populations is a priority task in amphibian conservation (Jiménez & Sommer, 2017;Trevelline, Fontaine, Hartup, & Kohl, 2019).…”

Section: Introductionmentioning

confidence: 99%

Association between the skin microbiome and MHC class II diversity in an amphibian

Cortázar-Chinarro

Richter‐Boix

Rödin‐Mörch

et al. 2023

Preprint

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It has become clear that the microbiome plays an important role in determining host health, diseases, and phenotypic variation. There is increasing evidence that the microbiome influences host fitness and its adaptation to the environment is changing our thinking on host-microbe interactions. However, it remains unclear how a host genotype shapes its microbiome. Here, we explored how genetic background and evolutionary history influence associated microbiome in amphibian populations. We studied how skin bacterial diversity is associated with the Major Histocompatibility Complex (MHC) class II exon 2 diversity in 12 moor frog populations belonging to two geographical clusters that show signatures of past and ongoing differential selection patterns. We found that bacterial alpha-diversity remained similar between the two clusters, while MHC haplotype-supertypes and genetic diversity differed between the clusters. Bacterial alpha-diversity was positively correlated with expected MHC heterozygosity and negatively with MHC nucleotide diversity. We also found that bacterial community composition differed significantly between the two geographic clusters and between specific MHC supertypes. These findings further suggest that population historical demographic events influence hologenomic variation and provide new insights into how immunogenetic host variability and microbial diversity may jointly influence host fitness with consequences for disease susceptibility and population persistence.

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Linking pathogen–microbiome–host interactions to explain amphibian population dynamics

Cited by 12 publications

References 104 publications

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Habitat split as a driver of disease in amphibians

Association between the skin microbiome and MHC class II diversity in an amphibian

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