Life history linked to immune investment in developing amphibians

Abstract

The broad diversity of amphibian developmental strategies has been shaped, in part, by pathogen pressure, yet trade-offs between the rate of larval development and immune investment remain poorly understood. The expression of antimicrobial peptides (AMPs) in skin secretions is a crucial defense against emerging amphibian pathogens and can also indirectly affect host defense by influencing the composition of skin microbiota. We examined the constitutive or induced expression of AMPs in 17 species at multiple life-history stages. We found that AMP defenses in tadpoles of species with short larval periods (fast pace of life) were reduced in comparison with species that overwinter as tadpoles and grow to a large size. A complete set of defensive peptides emerged soon after metamorphosis. These findings support the hypothesis that species with a slow pace of life invest energy in AMP production to resist potential pathogens encountered during the long larval period, whereas species with a fast pace of life trade this investment in defense for more rapid growth and development.

Keywords: Antimicrobial peptides; MALDI-TOF mass spectrometry; disease ecology; innate immunity; life-history strategy; tadpoles.

Figure 1:

Peptide profiles from four skin surfaces of adult Lithobates pipiens upon induction of granular gland secretions. Representative spectra of 10 replicates are shown.

Figure 2:

Representative skin peptide profiles of tadpoles and adults of five anuran species. Adult and metamorph spectra matched closely, and only adult profiles are displayed for clarity.

Figure 3:

Species sampled and tadpole characteristics. (A) Maximal tadpole length as reported in species descriptions (AmphibiaWeb, 2016). Species with large tadpoles that tend to overwinter and are categorized here as ‘slow pace-of-life’ species (dark blue). (B) Neighbour-joining tree of taxa tested in this study. The analysis involved 29 nucleotide sequences of the 16S rRNA gene. The final data set consists of 439 aligned nucleotide positions. Distances were computed using the p-distance method and are in the units of the number of base differences per site. Analyses were conducted in MEGA7 (Kumar et al., 2016). Species with tadpoles expressing AMPs (green circles) are not exclusively found within a single family.