Strong Bottlenecks Constrain Adaptive Coevolution in a Host-Parasite Metapopulation

Area of Science:

• Evolutionary Biology
• Parasitology
• Population Genetics

Background:

• Parasites adaptively evolve to exploit hosts.
• Transmission bottlenecks and host population structure can induce genetic drift in parasites, limiting their adaptive evolution.
• The interplay between host population dynamics and parasite evolution remains incompletely understood.

Purpose of the Study:

• To investigate the influence of host population structure on the genomic evolution of the microsporidian parasite Hamiltosporidium tvaerminnensis.
• To analyze the co-evolutionary dynamics between H. tvaerminnensis and its host, Daphnia magna, within a dynamic metapopulation.
• To determine if host population structure accelerates genetic drift in parasite populations.

Main Methods:

• Longitudinal whole-genome allele frequency tracking of 59 host (Daphnia magna) and parasite (Hamiltosporidium tvaerminnensis) subpopulations over 10 years.
• Analysis of co-dispersal and isolation-by-distance patterns between host and parasite.
• Identification of genetic signatures, including runs of homozygosity (ROHs), in parasite populations.

Main Results:

• Both host and parasite exhibited co-dispersal and isolation-by-distance, but host allele frequencies were more dynamic, showing recurrent genetic bottlenecks.
• Parasite populations displayed high shared heterozygosity but also subpopulation-specific runs of homozygosity (ROHs).
• Host population structure and metapopulation dynamics leave a traceable genomic signature in the parasite, suggesting accelerated drift.

Conclusions:

• Host population structure and metapopulation dynamics significantly shape parasite genomic evolution.
• Host-mediated parasite population bottlenecks can lead to the fixation of deleterious ROHs in parasite subpopulations.
• Contrary to expectations, parasites may evolve more slowly than their hosts, with host dynamics potentially accelerating parasite drift.