Adaptive evolution of major histocompatibility complex class I immune genes and disease associations in coastal juvenile sea turtles

Abstract

Characterizing polymorphism at the major histocompatibility complex (MHC) genes is key to understanding the vertebrate immune response to disease. Despite being globally afflicted by the infectious tumour disease fibropapillomatosis (FP), immunogenetic variation in sea turtles is minimally explored. We sequenced the α 1 peptide-binding region of MHC class I genes (162 bp) from 268 juvenile green ( Chelonia mydas ) and 88 loggerhead ( Caretta caretta ) sea turtles in Florida, USA. We recovered extensive variation (116 alleles) and trans-species polymorphism. Supertyping analysis uncovered three functional MHC supertypes corresponding to the three well-supported clades in the phylogeny. We found significant evidence of positive selection at seven amino acid sites in the class I exon. Random forest modelling and risk ratio analysis of Ch. mydas alleles uncovered one allele weakly associated with smooth FP tumour texture, which may be associated with disease outcome. Our study represents the first characterization of MHC class I diversity in Ch. mydas and the largest sample of sea turtles used to date in any study of adaptive genetic variation, revealing tremendous genetic variation and high adaptive potential to viral pathogen threats. The novel associations we identified between MHC diversity and FP outcomes in sea turtles further highlight the importance of evaluating genetic predictors of disease, including MHC and other functional markers.

Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

“…Although this viral-mediated tumor disease occurs in all sea turtle species, prevalence and recovery greatly vary between and within species, making it plausible that harboring certain genes, copy numbers, or specific alleles may play important roles in disease dynamics. Despite decades of research on this disease ( 30 ) only one study on the immunogenomic factors governing FP susceptibility or resilience has been conducted ( 81 ), in part due to difficulty in accurately quantifying hypervariable and complex MHC loci with short-read sequencing technologies ( 82 ). Our reference genomes now enable studies to accurately interrogate these complex gene families to advance our fundamental understanding of immune gene evolution in testudines.…”

Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

“…Although this likely viral-mediated tumor disease occurs in all sea turtle species, disease prevalence and recovery greatly varies between and within species, making it plausible that harboring certain genes, copy numbers, or specific alleles may play important roles in disease dynamics. Despite decades of research on this disease (30) only one study on the immunogenomic factors governing FP susceptibility or resilience has been conducted (81), in part due to difficulty in accurately quantifying hypervariable and complex MHC loci with short-read sequencing technologies (82). Our reference genomes now enable studies to accurately interrogate MHC and other immune genes to close this critical research gap and advance our fundamental understanding of immune gene evolution in testudines.…”

A Coupled Human and Natural Systems Framework to Characterize Emerging Infectious Diseases—The Case of Fibropapillomatosis in Marine Turtles

“…These environmental changes have occurred in parallel with increasing FP outbreaks in wild sea turtles. Immune system gene variation and higher susceptibility among juvenile individuals might also be risk factors behind FP; however, immunogenetic-environmental interactions are still suggested to potentially be driving disease outbreaks [68]. Previous literature on FP environmental etiology provides evidence that certain impacts from coastal anthropogenic disturbance over time may have been drivers behind exacerbation of this epizootic [66].…”