Direct Measurement of the Mutation Rate and Its Evolutionary Consequences in a Critically Endangered Mollusk

Abstract

The rate at which mutations arise is a fundamental parameter of biology. Despite progress in measuring germline mutation rates across diverse taxa, such estimates are missing for much of Earth's biodiversity. Here, we present the first estimate of a germline mutation rate from the phylum Mollusca. We sequenced three pedigreed families of the white abalone Haliotis sorenseni, a long-lived, large-bodied, and critically endangered mollusk, and estimated a de novo mutation rate of 8.60 × 10-9 single nucleotide mutations per site per generation. This mutation rate is similar to rates measured in vertebrates with comparable generation times and longevity to abalone, and higher than mutation rates measured in faster-reproducing invertebrates. The spectrum of de novo mutations is also similar to that seen in vertebrate species, although an excess of rare C > A polymorphisms in wild individuals suggests that a modifier allele or environmental exposure may have once increased C > A mutation rates. We use our rate to infer baseline effective population sizes (Ne) across multiple Pacific abalone and find that abalone persisted over most of their evolutionary history as large and stable populations, in contrast to extreme fluctuations over recent history and small census sizes in the present day. We then use our mutation rate to infer the timing and pattern of evolution of the abalone genus Haliotis, which was previously unknown due to few fossil calibrations. Our findings are an important step toward understanding mutation rate evolution and they establish a key parameter for conservation and evolutionary genomics research in mollusks.

Keywords: conservation; mollusk; mutation rate; phylogenomics.

Fig. 1.

Distribution of all SNV germline mutation rate estimates for multicellular eukaryotes, adapted from Wang and Obbard (2023). Multiple points per taxon represent multiple estimates of the GMR in that group. Time-scaled phylogeny to the left retrieved from TimeTree (Kumar et al. 2017).

Fig. 2.

a) Proportion of mutation types for all DNMs detected in pedigree sequencing. b) Proportion of single nucleotide polymorphisms (SNPs) in 11 wild-caught individuals as a function of minor allele frequency and polymorphism type.

Fig. 3.

a) Historical effective population size (N_e) for five abalone species as estimated by MSMC2 (Schiffels and Wang 2020). Both original data and 20 bootstrap replicates per species are shown. b) Distribution of intraspecific nucleotide diversity ($\mathrm{\pi }$) for species where multiple sequenced individuals were available. Effective population size is calculated from $\mathrm{\pi }$ = 4N_eμ using the mean observed $\mathrm{\pi }$.

Fig. 4.

a) Multispecies coalescent (MSC) phylogeny inferred with BPP (Flouri et al. 2018) and calibrated assuming μ.mean = 8.60 × 10⁻⁹, μ.sd = 3.26 × 10⁻⁹, g.mean = 6, and g.sd = 2, where μ is the mutation rate and g is the generation time. The tree is rooted with the outgroup G. magus, not shown. b) Distributions of the six abalone species presented in Fig. 3a. Range maps obtained from the IUCN Red List.