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Hybrid advantage in skin peptide immune defenses of water frogs (Pelophylax esculentus) at risk from emerging pathogens


Daum, Janine M; Davis, Leyla R; Bigler, Laurent; Woodhams, Doug C (2012). Hybrid advantage in skin peptide immune defenses of water frogs (Pelophylax esculentus) at risk from emerging pathogens. Infection, Genetics and Evolution, 12(8):1854-1864.

Abstract

Heterogeneity in immune defense effectors can benefit hosts encountering a variety of parasites and pathogens. Antimicrobial peptides (AMPs) are a diverse set of immune defense effectors in many amphib- ians, and are secreted from dermal granular glands to protect the skin from infection. Over 50 different skin peptides have been reported from the European water frog hybridogenic complex (Pelophylax escu- lentus complex), consisting of the hybrid P. esculentus, and the parent species Pelophylax lessonae and Pelo- phylax ridibundus. In central Europe the hybrid is sympatric with only P. lessonae, while in other areas all three species can co-occur. Amphibian immune defenses are likely under selective pressure from emerg- ing pathogens such as the chytrid fungus Batrachochytrium dendrobatidis (Bd). To assess if hybridization affects immune defenses against Bd, we compared skin peptides of the three species in terms of (i) quan- tity, (ii) activity against Bd, (iii) repertoire, and (iv) stability. Hybrids secreted AMPs at higher quantities and with greater fungicidal activity compared to cohabiting P. lessonae. Compared to P. ridibundus, AMPs from hybrids were of similar quantity but slightly greater antifungal activity. Mass spectrometric analy- ses (MALDI-TOF) revealed that of all three species P. esculentus has the greatest peptide diversity, a rep- ertoire inclusive of peptides occurring in either one or the other parent species. Measurements of degradation dynamics indicate that peptides remain relatively stable on the skin of all species for over an hour after induction of skin gland secretions. Our data demonstrate that the hybrid has more effective peptide defenses against Bd and a richer peptide repertoire than either parent species. Hybrid advantage in environments hosting virulent pathogens may contribute to disassortative mating preferences, and we suggest that AMP diversity may be analogous to major histocompatibility complex (MHC) heterozygosity by benefiting hosts encountering multiple parasites.

Abstract

Heterogeneity in immune defense effectors can benefit hosts encountering a variety of parasites and pathogens. Antimicrobial peptides (AMPs) are a diverse set of immune defense effectors in many amphib- ians, and are secreted from dermal granular glands to protect the skin from infection. Over 50 different skin peptides have been reported from the European water frog hybridogenic complex (Pelophylax escu- lentus complex), consisting of the hybrid P. esculentus, and the parent species Pelophylax lessonae and Pelo- phylax ridibundus. In central Europe the hybrid is sympatric with only P. lessonae, while in other areas all three species can co-occur. Amphibian immune defenses are likely under selective pressure from emerg- ing pathogens such as the chytrid fungus Batrachochytrium dendrobatidis (Bd). To assess if hybridization affects immune defenses against Bd, we compared skin peptides of the three species in terms of (i) quan- tity, (ii) activity against Bd, (iii) repertoire, and (iv) stability. Hybrids secreted AMPs at higher quantities and with greater fungicidal activity compared to cohabiting P. lessonae. Compared to P. ridibundus, AMPs from hybrids were of similar quantity but slightly greater antifungal activity. Mass spectrometric analy- ses (MALDI-TOF) revealed that of all three species P. esculentus has the greatest peptide diversity, a rep- ertoire inclusive of peptides occurring in either one or the other parent species. Measurements of degradation dynamics indicate that peptides remain relatively stable on the skin of all species for over an hour after induction of skin gland secretions. Our data demonstrate that the hybrid has more effective peptide defenses against Bd and a richer peptide repertoire than either parent species. Hybrid advantage in environments hosting virulent pathogens may contribute to disassortative mating preferences, and we suggest that AMP diversity may be analogous to major histocompatibility complex (MHC) heterozygosity by benefiting hosts encountering multiple parasites.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
07 Faculty of Science > Department of Chemistry
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
540 Chemistry
Uncontrolled Keywords:Amphibian; Antimicrobial peptides; Batrachochytrium dendrobatidis; Chytridiomycosis; MALDI-MS; Rana esculenta
Language:English
Date:2012
Deposited On:23 Jan 2013 11:27
Last Modified:05 Apr 2016 16:19
Publisher:Elsevier
ISSN:1567-1348
Publisher DOI:https://doi.org/10.1016/j.meegid.2012.07.024
PubMed ID:22940461

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