Influence of immunogenetics, sex and body condition on the cutaneous microbial communities of two giant salamanders

Abstract

The complex association between hosts and microbial symbionts requires the implementation of multiple approaches to evaluate variation in host physiology. Within amphibians, heterogeneity in immunogenetic traits and cutaneous microbiota is associated with variation in disease resistance. Ozark (Cryptobranchus alleganiensis bishopi) and eastern hellbenders (C. a. alleganiensis) provide a model system to assess variation in host traits and microbial communities. Ozark hellbenders have experienced declines throughout their range, are federally endangered and experience wound retardation that is absent in the eastern subspecies. Previous microbial investigations indicate differentiation in the composition of the skin microbiota of both hellbender subspecies, but it is not clear whether these patterns are concurrent with diversity in the major histocompatibility complex (MHC) genes. We characterized the MHC IIB and the skin microbiota of hellbenders in Missouri, where both subspecies co-occur though not sympatric. We compared the microbiota composition and MHC diversity between both subspecies and investigated whether individual-level MHC diversity, sex and body condition were associated with microbiota composition. Overall, MHC IIB diversity was lower in Ozark hellbenders compared to the eastern subspecies. Multivariate statistical comparisons identified microbiota differentiation between Ozark and eastern hellbenders. MHC IIB allele presence/absence, allele divergence, body composition and sex defined grouping of hellbender microbiotas within populations. Differentiation of the cutaneous microbiotas and MHC IIB genes between eastern and Ozark hellbenders suggests that differences exist in immunity between the two subspecies. This study demonstrates how simultaneous assessments of host genetic traits and microbiotas can inform patterns of microbial community structure in natural systems.

Evaluation of Severity and Factors Contributing to Foot Lesions in Endangered Ozark Hellbenders, Cryptobranchus alleganiensis bishopi

“…Low immunogenetic diversity is linked to increased disease incidence in other wildlife species e.g., malaria in great reed warblers (57), and facial tumors in Tasmanian Devils (58). C a. bishopi have lower MHC IIb diversity than their Eastern counter parts in Missouri (59) and combined with other factors, may have reached a threshold to become less resistant to one or more pathogens. Further, genetic bottlenecking could also increase frequency of rare alleles and chances for genetically driven disease.…”

Editorial 2019

“…The second section featured a number of manuscripts that investigated the structure of the microbiome in an attempt to understand the drivers of microbiota community assembly and turnover. Some contributions weighed in on the role of host phylogeny vs. ecology (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ; Ivens, Gadau, Kiers, & Kronauer, 2018; Hernandez‐Gomez, Briggler, & Williams, ; Kohl, Dearing, & Bordenstein, ; Nishida & Ochman, ; Roth‐Schulze et al., ; Schuelke, Pereira, Hardy, & Bik, ), others probed how the presence of hosts themselves alters the microbiota around them (Chen & Parfrey, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ), one investigated patterns of co‐infection (Rock et al, ) and one documented changes in microbiota during development (Prest, Kimball, Kueneman, & McKenzie, ). A few studies in this section studied the structure of the microbiome with manipulative experiments (e.g., Chen & Parfrey, ; Erlandson et al, ; Morella, Gomez, Wang, Leung, & Koskella, ; Raymann, Bobay, & Moran, ).…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…The plausible expression of the encoded MHCIIb proteins on salamander skin is argued to enable direct interactions between these molecules and the microbiota. The authors show that the salamander subspecies are distinct in microbiota and MHC profiles (Hernández‐Gómez, Briggler, & Williams, ). Most importantly, they find that divergence in MHC at the amino acid level, and differential presence/absence of specific MHC alleles, significantly predict a portion of interindividual microbiome variability within populations (Hernández‐Gómez et al., ).…”

“…The authors show that the salamander subspecies are distinct in microbiota and MHC profiles (Hernández‐Gómez, Briggler, & Williams, ). Most importantly, they find that divergence in MHC at the amino acid level, and differential presence/absence of specific MHC alleles, significantly predict a portion of interindividual microbiome variability within populations (Hernández‐Gómez et al., ). In mice, MHC‐induced changes in bacterial composition alter disease susceptibility (Kubinak et al., ), suggesting the importance for this discovery in the disease ecology of endangered amphibian species.…”