The Metabolic Pace-of-Life Model: Incorporating Ectothermic Organisms into the Theory of Vertebrate Ecoimmunology

We propose a new heuristic model that incorporates metabolic rate and pace of life to predict a vertebrate species’ investment in adaptive immune function. Using reptiles as an example, we hypothesize that animals with low metabolic rates will invest more in innate immunity compared with adaptive immunity. High metabolic rates and body temperatures should logically optimize the efficacy of the adaptive immune system—through rapid replication of T and B cells, prolific production of induced antibodies, and kinetics of antibody–antigen interactions. In current theory, the precise mechanisms of vertebrate immune function oft are inadequately considered as diverse selective pressures on the evolution of pathogens. We propose that the strength of adaptive immune function and pace of life together determine many of the important dynamics of host–pathogen evolution, namely, that hosts with a short lifespan and innate immunity or with a long lifespan and strong adaptive immunity are expected to drive the rapid evolution of their populations of pathogens. Long-lived hosts that rely primarily on innate immune functions are more likely to use defense mechanisms of tolerance (instead of resistance), which are not expected to act as a selection pressure for the rapid evolution of pathogens’ virulence

Tortoise sample data file

Data file including information on each tortoise sampled, presence or absence of pathogens in the samples, and barcode sequences for pyrosequencing. Includes sheet of column descriptions

OTU biom table

OTU biom table of bacteria in the upper respiratory tracts of 146 North American tortoises. Biom table includes only bacterial OTUs and excludes OTUs represented by only one sequence

An ecoimmunological approach to disease in tortoises reveals the importance of lymphocytes

We quantified the severity of upper respiratory tract disease (URTD) and immunological metrics (differential white blood cell counts and bacteria-killing ability of blood plasma) in relation to climatic variables in 20 populations of Mojave desert tortoise (Gopherus agassizii). Prevalence and infection intensity of Mycoplasma agassizii, an etiological agent of URTD, have previously been quantified for these populations (Weitzman et al. 2017). Immunological variables were reduced by principal component analyses and separated into cells involved in inflammation (PC1) and cellular functions mediated by lymphocytes and basophils (PC2). In population-level models, the mean number of lymphocytes per individual was associated with mean annual number of days below freezing. Lymphocytes were also positively associated with mean infection intensity of M. agassizii. Additionally, prevalence of URTD was closely associated with PC1 (cells associated with inflammation). This suggests that at least two immunological strategies are involved in responding to M.agassizii, one that involves primarily lymphocytes and one that involves inflammatory mechanisms. Recent studies on immunology in Testudines suggest that a large proportion of lymphocytes in this taxon are similar to B-1 lymphocytes of mammals and have phagocytic properties. Controlled experiments are needed to understand the disease mitigation of these lymphocytes in desert tortoises

Data from: Host species, pathogens, and disease associated with divergent nasal microbial communities in tortoises

Diverse bacterial communities are found on every surface of macro-organisms, and they play important roles in maintaining normal physiological functions in their hosts. While the study of microbiomes has expanded with the influx of data enabled by recent technological advances, microbiome research in reptiles lags behind other organisms. We sequenced the nasal microbiomes in a sample of four North American tortoise species, and we found differing community compositions among tortoise species and sampling sites, with higher richness and diversity in Texas and Sonoran desert tortoises. Using these data, we investigated the prevalence and operational taxonomic unit (OTU) diversity of the potential pathogen Pasteurella testudinis, and found it to be common, abundant, and highly diverse. However, the presence of this bacterium was not associated with differences in bacterial community composition within host species. We also found that the presence of nasal discharge from tortoises at the time of sampling was associated with a decline in diversity and a change in microbiome composition, which we posit is due to the harsh epithelial environment associated with immune responses. Repeated sampling across seasons, and at different points of pathogen colonisation, should contribute to our understanding of the causes and consequences of different bacterial communities in these long-lived hosts

A trade-off between natural and acquired antibody production in a reptile: implications for long-term resistance to disease

Vertebrate immune systems are understood to be complex and dynamic, with trade-offs among different physiological components (e.g., innate and adaptive immunity) within individuals and among taxonomic lineages. Desert tortoises (Gopherus agassizii) immunised with ovalbumin (OVA) showed a clear trade-off between levels of natural antibodies (NAbs; innate immune function) and the production of acquired antibodies (adaptive immune function). Once initiated, acquired antibody responses included a long-term elevation in antibodies persisting for more than one year. The occurrence of either (a) high levels of NAbs or (b) long-term elevations of acquired antibodies in individual tortoises suggests that long-term humoral resistance to pathogens may be especially important in this species, as well as in other vertebrates with slow metabolic rates, concomitantly slow primary adaptive immune responses, and long life-spans

A Trade-Off Between Natural and Acquired Antibody Production in a Reptile: Implications for Long-Term Resistance to Disease

Skip to Next Section Vertebrate immune systems are understood to be complex and dynamic, with trade-offs among different physiological components (e.g., innate and adaptive immunity) within individuals and among taxonomic lineages. Desert tortoises (Gopherus agassizii) immunised with ovalbumin (OVA) showed a clear trade-off between levels of natural antibodies (NAbs; innate immune function) and the production of acquired antibodies (adaptive immune function). Once initiated, acquired antibody responses included a long-term elevation in antibodies persisting for more than one year. The occurrence of either (a) high levels of NAbs or (b) long-term elevations of acquired antibodies in individual tortoises suggests that long-term humoral resistance to pathogens may be especially important in this species, as well as in other vertebrates with slow metabolic rates, concomitantly slow primary adaptive immune responses, and long life-spans

Co-infection does not predict disease signs in Gopherus tortoises

In disease ecology, the host immune system interacts with environmental conditions and pathogen properties to affect the impact of disease on the host. Within the host, pathogens may interact to facilitate or inhibit each other's growth, and pathogens interact with different hosts differently. We investigated co-infection of two Mycoplasma and the association of infection with clinical signs of upper respiratory tract disease in four congeneric tortoise host species (Gopherus) in the United States to detect differences in infection risk and disease dynamics in these hosts. Mojave Desert tortoises had greater prevalence of Mycoplasma agassizii than Texas tortoises and gopher tortoises, while there were no differences in Mycoplasma testudineum prevalence among host species. In some host species, the presence of each pathogen influenced the infection intensity of the otherhence, these two mycoplasmas interact differently within different hosts, and our results may indicate facilitation of these bacteria. Neither infection nor co-infection was associated with clinical signs of disease, which tend to fluctuate across time. From M. agassizii DNA sequences, we detected no meaningful differentiation of haplotypes among hosts. Experimental inoculation studies and recurrent resampling of wild individuals could help to decipher the underlying mechanisms of disease dynamics in this system

High quality draft genome sequence of &ITMycoplasma testudineum&IT strain BH29(T), isolated from the respiratory tract of a desert tortoise

Mycoplasma testudineum is one of the pathogens that can cause upper respiratory tract disease in desert tortoises, Gopherus agassizii. We sequenced the genome of M. testudineum BH29(T) (ATCC 700618(T) = MCCM 03231(T)), isolated from the upper respiratory tract of a Mojave desert tortoise with upper respiratory tract disease. The sequenced draft genome, organized in 25 scaffolds, has a length of 960,895 bp and a G + C content of 27.54%. A total of 788 protein-coding sequences, six pseudogenes and 35 RNA genes were identified. The potential presence of cytadhesin-encoding genes is investigated. This genome will enable comparative genomic studies to help understand the molecular bases of the pathogenicity of this and other Mycoplasma species