Gene genealogies strongly distorted by weakly interfering mutations in constant environments

Area of Science:

• Evolutionary Biology
• Population Genetics
• Molecular Evolution

Background:

• Neutral nucleotide diversity typically scales with population size, but this is not observed in animal mitochondria, a phenomenon known as the "paradox of variation."
• Adaptive selective sweeps are a common explanation, but interference among deleterious mutations offers a plausible alternative.

Purpose of the Study:

• To investigate the "paradox of variation" in animal mitochondrial DNA.
• To test the hypothesis that Hill-Robertson interference among deleterious mutations explains observed mitochondrial genealogies.
• To model the impact of linked deleterious mutations on nucleotide diversity and genealogical patterns.

Main Methods:

• Analysis of mitochondrial genealogies in whale lice (Amphipoda: Cyamus).
• Development and application of a coalescent simulation algorithm to model interference among mutations.
• Exploration of a wide range of parameter values, including selection coefficients and population size.

Main Results:

• Mitochondrial genealogies of whale lice were consistently shorter and distorted in shape and topology compared to neutral expectations.
• These patterns were reproduced by models of interference among forward and back mutations on a nonrecombining chromosome.
• Genealogical distortions were maximized under intermediate selection coefficients, nearing Muller's ratchet threshold.
• Linked neutral nucleotide diversity became largely insensitive to population size (N) in this regime.

Conclusions:

• Hill-Robertson interference among a large number of weakly deleterious mutations provides a compelling explanation for the paradox of variation in animal mitochondria.
• This interference mechanism leads to a generalized background-selection model, reducing effective population size over evolutionary time.
• The findings challenge solely adaptive explanations and highlight the significant role of linked deleterious mutation interference in shaping molecular evolution.