Pathogen-mediated selection favours the maintenance of innate immunity gene polymorphism in a widespread wild ungulate.

Toll-like receptors (TLR) play a central role in recognition and host frontline defence against a wide range of pathogens. A number of recent studies have shown that TLR genes (Tlrs) often exhibit large polymorphism in natural populations. Yet, there is little knowledge on how this polymorphism is maintained and how it influences disease susceptibility in the wild. In previous work, we showed that some Tlrs exhibit similarly high levels of genetic diversity as genes of the Major Histocompatibility Complex (MHC), and signatures of contemporary balancing selection in roe deer (Capreolus capreolus), the most abundant cervid species in Europe. Here, we investigated the evolutionary mechanisms by which pathogen-mediated selection could shape this innate immunity genetic diversity by examining the relationships between Tlr (Tlr2, Tlr4 and Tlr5) genotypes (heterozygosity status and presence of specific alleles) and infections with Toxoplasma and Chlamydia, two widespread intracellular pathogens known to cause reproductive failure in ungulates. We showed that Toxoplasma and Chlamydia exposures vary significantly across years and landscape features with few co-infection events detected and that the two pathogens exert antagonistic selection on Tlr2 polymorphism. By contrast, we found limited support for Tlr heterozygote advantage. Our study confirmed the importance of looking beyond Mhc genes in wildlife immunogenetic studies. It also emphasized the necessity to consider multiple pathogen challenges and their spatiotemporal variation to improve our understanding of vertebrate defence evolution against pathogens.

Evolution and Adaptation of Forest and Crop Pathogens in the Anthropocene.

Anthropocene marks the era when human activity is making a significant impact on earth, its ecological and biogeographical systems. The domestication and intensification of agricultural and forest production systems have had a large impact on plant and tree health. Some pathogens benefitted from these human activities and have evolved and adapted in response to the expansion of crop and forest systems, resulting in global outbreaks. Global pathogen genomics data including population genomics and high-quality reference assemblies are crucial for understanding the evolution and adaptation of pathogens. Crops and forest trees have remarkably different characteristics, such as reproductive time and the level of domestication. They also have different production systems for disease management with more intensive management in crops than forest trees. By comparing and contrasting results from pathogen population genomic studies done on widely different agricultural and forest production systems, we can improve our understanding of pathogen evolution and adaptation to different selection pressures. We find that in spite of these differences, similar processes such as hybridization, host jumps, selection, specialization, and clonal expansion are shaping the pathogen populations in both crops and forest trees. We propose some solutions to reduce these impacts and lower the probability of global pathogen outbreaks so that we can envision better management strategies to sustain global food production as well as ecosystem services.

Hybridization and introgression drive genome evolution of Dutch elm disease pathogens.

Hybridization and the resulting introgression can drive the success of invasive species via the rapid acquisition of adaptive traits. The Dutch elm disease pandemics in the past 100 years were caused by three fungal lineages with permeable reproductive barriers: Ophiostoma ulmi, Ophiostoma novo-ulmi subspecies novo-ulmi and Ophiostoma novo-ulmi subspecies americana. Using whole-genome sequences and growth phenotyping of a worldwide collection of isolates, we show that introgression has been the main driver of genomic diversity and that it impacted fitness-related traits. Introgressions contain genes involved in host-pathogen interactions and reproduction. Introgressed isolates have enhanced growth rate at high temperature and produce different necrosis sizes on an in vivo model for pathogenicity. In addition, lineages diverge in many pathogenicity-associated genes and exhibit differential mycelial growth in the presence of a proxy of a host defence compound, implying an important role of host trees in the molecular and functional differentiation of these pathogens.