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PLoS Genet
2024 Feb 01;202:e1011129. doi: 10.1371/journal.pgen.1011129.
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High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.
Popovic I
,
Bergeron LA
,
Bozec YM
,
Waldvogel AM
,
Howitt SM
,
Damjanovic K
,
Patel F
,
Cabrera MG
,
Wörheide G
,
Uthicke S
,
Riginos C
.
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Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (Nc) variation, is an evolutionary conundrum. The most extreme mismatches between π and Nc are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as Nc fluctuations are unknown. Here, we provide the first germline mutation rate (μ) estimate for a marine invertebrate in corallivorous crown-of-thorns sea stars (Acanthaster cf. solaris). We use high-coverage whole-genome sequencing of 14 parent-offspring trios alongside empirical estimates of Nc in Australia's Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme Nc fluctuations. The A. cf. solaris mean μ was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08), exceeding estimates for other invertebrates and showing greater concordance with vertebrate mutation rates. Lower-than-expected Ne (~70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated weak influences of population outbreaks on long-term π. Our findings are consistent with elevated μ evolving in response to reduced Ne and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.
Fig 1. Conceptual diagram illustrating the relationships between evolutionary parameters underlying genetic diversity.Under mutation-drift equilibrium, pairwise genetic diversity (π) reflects the balance between new mutations (μ) and the loss of variation via genetic drift, reflected by effective population size (Ne). In natural populations, π does not increase linearly with Ne and Ne is often smaller than census population size (Nc). μ is unknown for marine invertebrate taxa, thus the contributions of new mutations to π remain unknown. The drift-barrier hypothesis, a leading explanation for μ variation, proposes that selection against high μ is less efficient in small Ne species. This leads to an inverse relationship between μ and Ne (μ ~1/2Ne for diploid organisms) and the evolution of high μ in small Ne populations. Key evolutionary and ecological processes or traits affecting the magnitude of each parameter are shown. Several evolutionary processes act in combination to reduce Ne and thus, constrain π, decoupling it from Nc. This decoupling leads to a disparity between the range of π and Nc variance observed across taxa, known as Lewontin’s paradox. π can be measured in natural populations using DNA sequencing to calculate pairwise differences between sampled individuals and Nc can be approximated most accurately from direct observations of organisms from field surveys. μ and Ne are inferred parameters from polymorphism data.
Fig 2. Germline mutation rates inferred in Acanthaster cf. solaris and other metazoan taxa.Top panel: Germline mutation rates (μ) for 14 A. cf. solaris parent-offspring trios. Individual estimates for each trio are shown in grey. The average μ is show in black and 95% confidence intervals are indicated with error bars. Lower panel: Previously published average μ estimates and 95% confidence intervals for representative metazoan groups. Mutation rates estimates from [16] are represented by squares and estimates from other publications (both pedigree-based and mutation accumulation approaches) are represented by circles. 95% confidence intervals are shown as reported or omitted if not reported. In cases where multiple estimates are available for a single taxon, 95% confidence intervals from the most recent publication are shown. Refer to S9 Table for article details. Exceedingly high mutation rate estimates (μ > 2.5 x 10−08) for Thamnophis sirtalis and Rhea pennata [16] (S9 Table) are omitted for visual purposes only. Silhouettes were sourced from Phylopic (http://phylopic.org).
Fig 3. Historical Ne trajectories inferred in MSMC2 applying the inferred Acanthaster cf. solaris mutation rate and nucleotide diversity from 14 parental genomes (four parental haplotypes per larva).Populations have experienced large fluctuations over the past 10,000 to 1 million years, with peak population sizes ~60,000 years ago and a most recent minimum ~20,000 years ago coinciding with the lowest global sea levels during the late Pleistocene [79]. The long-term harmonic Ne between the last 10,000 to 1 million years (~180,000) is indicated by the grey dashed line.
Fig 4. Recent adult Acanthaster cf. solaris abundance estimates in the Great Barrier Reef (GBR) based on long-term monitoring data.(A) Individual reefs monitored between 1991 and 2022; (B) Contemporary abundance estimates of adult A. cf. solaris across the GBR (3,054 reefs). For each surveyed reef, individual A. cf. solaris counts were converted into a density estimate (individuals km-2), where mean reef-level density was calculated for each annual sample and a 95% confidence interval of annual mean densities was calculated from 500 pseudo-samples generated by bootstrap for each year. The confidence limits and the mean of the annual mean densities were multiplied by the total surface area of the preferred A. cf. solaris habitat of reef-building corals on the GBR to calculate census population size. Black dots indicate the average abundance, while vertical lines indicate the extent of the 95% confidence intervals of the 500 mean annual values estimated by bootstrap sampling. The blue and red dashed lines represent, respectively, the harmonic means of the 2.5th (6.7 million) and 97.5th percentiles (14.3 million) of mean annual values over 32 years of monitoring. https://geoportal.gbrmpa.gov.au/.
