Specific MHC class I supertype associated with parasite infection and color morph in a wild lizard population

Abstract

The major histocompatibility complex (MHC) is a large gene family that plays a central role in the immune system of all jawed vertebrates. Nonavian reptiles are underrepresented within the MHC literature and little is understood regarding the mechanisms maintaining MHC diversity in this vertebrate group. Here, we examined the relative roles of parasite-mediated selection and sexual selection in maintaining MHC class I diversity of a color polymorphic lizard. We discovered evidence for parasite-mediated selection acting via rare-allele advantage or fluctuating selection as ectoparasite load was significantly lower in the presence of a specific MHC supertype (functional clustering of alleles): supertype four. Based on comparisons between ectoparasite prevalence and load, and assessment of the impact of ectoparasite load on host fitness, we suggest that supertype four confers quantitative resistance to ticks or an intracellular tickborne parasite. We found no evidence for MHC-associated mating in terms of pair genetic distance, number of alleles, or specific supertypes. An association was uncovered between supertype four and male throat color morph. However, it is unlikely that male throat coloration acts as a signal of MHC genotype to conspecifics because we found no evidence to suggest that male throat coloration predicts male mating status. Overall, our results suggest that parasite-mediated selection plays a role in maintaining MHC diversity in this population via rare-allele advantage and/or fluctuating selection. Further work is required to determine whether sexual selection also plays a role in maintaining MHC diversity in agamid lizards.

Keywords: Agamidae; Ctenophorus decresii; MHC‐associated mating; major histocompatibility complex; parasite‐mediated selection.

Figure 1

A male tawny dragon lizard (Ctenophorus decresii) at the Hawker field site in the Flinders Ranges, South Australia (a). An example of an adult male chest patch marking (b), and the four throat color morphs present within the Hawker population, ordered left to right from most frequent to least frequent (c)

Figure 2

Relationship between the presence and absence of supertype four and tick prevalence (a) and mean (±SE) tick load (b), and the relationship between tick load and body condition (showing 95% confidence intervals with shaded area and dotted lines), comparing individuals with and without supertype four (c)

Figure 3

Difference between available and mated Ctenophorus decresii males in average pair percent difference among shared MHC I alleles (a) and male number of MHC I alleles (b). Mean values are indicated with a red point

Figure 4

Mean (±SE) percentage of male throat color (a: orange, b: yellow) as a function of supertype presence (only supertypes that were present in models with ΔAICc ≤ 2 are displayed) and the percentage of individuals of each male throat morph that possess supertype four (c)