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Chytridiomycosis resistance through sexual selection

Periodic Reporting for period 1 - CRISIS (Chytridiomycosis resistance through sexual selection)

Reporting period: 2022-05-01 to 2024-04-30

The last decades have seen an increase of emerging infectious diseases, in humans, livestock, and wildlife – the current Covid-19 pandemic being just one popular example. When investigating these diseases, researchers tend to focus on the pathogens, but the host also plays a critical role in the determination of infection outcome, for instance through immunity. Sexual selection is a strong evolutionary force that can facilitate or inhibit adaptation to environmental challenges. When populations face novel pathogens, sexual selection can influence their ability to persist by impacting the spread of traits that confer disease resistance. The major histocompatibility complex (MHC) encodes proteins that recognize pathogens and activate the immune system, allowing the organism to fight against the pathogen. Many vertebrates preferentially mate with partners that carry beneficial MHC alleles, conferring higher resistance to their offspring. By understanding the role of sexual in the evolution of disease resistance, we can better protect global diversity, and identify which species are in more dire need of conservation.

Currently, amphibians are one of the most threatened animal groups, with 41% of the species declining. This is of high concern for humans, as amphibians control the overgrowth of pests, are an important food source, and are the source of many medical advances. In addition to habitat destruction, the disease chytridiomycosis is a major cause of extinction. While it has been recently found that the MHC genes of individuals in infected populations is under strong selection, it is unclear which evolutionary force is driving it. Thus, understanding the evolutionary dynamics of MHC could be critical for preserving amphibian diversity. However, there is a lot of fundamental knowledge missing when it comes to the amphibian MHC, for instance, it is currently unknown whether MHC dependent mate choice occurs in amphibians. This makes them the perfect organism to study this issue.

In this project I explore the role of sexual selection in the evolutionary dynamics of amphibian resistance to chytridiomycosis (an emerging infectious disease that is causing population declines and extinctions worldwide) with poison frogs (a species-rich group in which the strength of sexual selection differs between species). I start by reviewing the current knowledge on the amphibian MHC. Then I test whether mate preferences are influenced by MHC or by the infection status of both partners. Finally, I use theoretical models to predict under which circumstances sexual selection can accelerate the evolution of disease resistance. This project provides fundamental scientific knowledge on the relationship between sexual selection and the evolution of disease immunity against an extremely lethal pathogen by exploring the interaction between chytridiomycosis and amphibian MHC. It builds on the recent insights that natural selection drives MHC evolution in amphibians, and originally explores the role of sexual selection in this process in a uniquely integrated experimental, theoretical, and ecological fashion.
Objective I - reviewing the current knowledge on the amphibian MHC
For this objective an extensive literature search was conducted which culminated in the combination of knowledge acquired in close to 300 scientific peer-reviewed scientific publications.
Information was divided into topics for reading simplicity, and the manuscript ends with a research agenda of topics that should be addressed in the coming years.
This review has been written and is currently under evaluation in a scientific journal.

Objective II - influence of MHC and infection status on mate preferences
For this objective two rounds of mate choice experiments were conducted in French Guiana and Panama. In these experiments females could choose between males which possessed different MHC alleles and infection status.
Data showed that females preferred males with different MHC alleles when uninfected, however this preference was lost when the females were infected.
This data has been disseminated at scientific meetings in Europe and America, and is currently being written up into a manuscript that will be submitted to a scientific journal.

Objective III - prediction of sexual selection driven evolution of disease resistance
For this objective a computer simulation was build to mimic a population of amphibians with complex behaviors, mate preferences, and immune systems.
Data showed that sexual selection had a minor role on the evolution of disease resistance, with the presence of parental care being the most relevant one.
This data has been disseminated at scientific meetings in Europe, and is currently being written up into a manuscript that will be submitted to a scientific journal.
This project has expanded on the current state of knowledge in two ways: 1) it showed that amphibians mate preferences are related to the resistance alleles. This was known to be true in most other vertebrate groups, and has now been shown to exist in amphibians too; 2) it revealed that sexual selection plays a minor role in the evolution of disease resistance to chytridiomycosis, and a high potential to increase disease spread. This goes against expectations and provides further explanation to why amphibians are so susceptible to this disease. Additionally, this project generated a review that summarizes current knowledge on the amphibian MHC which is useful to researchers from many fields and helps find consensus between seemly conflicting publications.
Subject - Pelophylax lessonae