Interaction between genetic variation and susceptibility to environmental challenge in Mediterranean dolphins

Abstract

Top predators such as marine mammals are particularly sensitive to perturbations in the ecosystem due to their longevity and food web position. The adaptation of wild animals to environmental change is thus crucial and facilitated by genetic diversity. Pathogens represent a significant mortality source in wild animals, with host resistance and survival being mediated by molecular mechanisms and genetic components. Since pathogens represent a strong selective pressure for their hosts and new pathogens are constantly introduced into host populations, such that pathogen dynamics are particularly good models to study adaptation.
The present study investigated the genetic diversity in the Mediterranean Sea, as well as the genomic basis of striped dolphin (Stenella coeruleoalba) vulnerability to morbillivirus disease – a highly contagious and deadly virus that infects mammals, and has been considered a serious ecological threat.
The striped dolphin has a world-wide distribution, and is the most abundant cetacean species in the Mediterranean Sea – the stage of several morbillivirus epizootic outbreaks over the past 33 years. This Delphinidae species has been reported as one of the most susceptible cetaceans to morbillivirus disease, and even possibly a reservoir for this virus, which could have serious implications for endangered species conservation.
To assess aspects that could be influencing the vulnerability of striped dolphin to morbillivirus infection, different approaches were taken in this study, including assessing connectivity and the association of death during epizootics with inbreeding/genotype analysis at susceptibility-related candidate genes. Patterns of genetic diversity and population structure can contribute to influence disease spread and species fitness. Thus, population structure was evaluated within the East and West regions of the Western Mediterranean basin, as well as between Mediterranean and Atlantic individuals. Using random genome-wide scans, measures of heterozygosity-fitness correlations, inbreeding, and potential candidate genes associated with morbillivirus susceptibility, were investigated for this species. Additionally, signs of selection associated with morbillivirus disease were also assessed using a hybridization-based capture procedure with specific genomic regions, including immune system related genes, as targets.
This study suggests stronger structure between Atlantic and Mediterranean individuals than between sampled regions within the Mediterranean region, suggesting high levels of connectivity within the western basin. Levels of inbreeding for the Mediterranean striped dolphin were low, and genome-wide heterozygosity were found to be within reported values for mammals. Genome-wide heterozygosity-fitness analyses did not reveal significant correlations between diversity levels and fitness associated with surviving morbillivirus infection. However, possible signs of morbillivirus susceptibility were found with the identification of particular loci with functions that were consistent with morbillivirus infection/disease. The targeted capture approach corroborated the absence of a clear general effect, even among multiple loci with shared immune system functions with only one locus (HAVCR2) showing a strong correlation with morbillivirus exposure.
These time-series data contribute to the scientific knowledge on striped dolphin susceptibility to morbillivirus disease, as well as its geographical diversity, conferring relevant information that could be useful to future studies and conservation measures for this species.