Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana

Julie A Koester,Walter L Ruzzo,Micaela S Parker,Rhonda Morales,Vaughn Iverson,Naozumi Hiranuma,Chris T Berthiaume,E Virginia Armbrust

doi:10.1038/s41598-018-28630-4

Abstract

Sexual reproduction roots the eukaryotic tree of life, although its loss occurs across diverse taxa. Asexual reproduction and clonal lineages persist in these taxa despite theoretical arguments suggesting that individual clones should be evolutionarily short-lived due to limited phenotypic diversity. Here, we present quantitative evidence that an obligate asexual lineage emerged from a sexual population of the marine diatom Thalassiosira pseudonana and rapidly expanded throughout the world’s oceans. Whole genome comparisons identified two lineages with characteristics expected of sexually reproducing strains in Hardy-Weinberg equilibrium. A third lineage displays genomic signatures for the functional loss of sexual reproduction followed by a recent global colonization by a single ancestral genotype. Extant members of this lineage are genetically differentiated and phenotypically plastic, potentially allowing for rapid adaptation when they are challenged by natural selection. Such mechanisms may be expected to generate new clones within marginal populations of additional unicellular species, facilitating the exploration and colonization of novel environments, aided by exponential growth and ease of dispersal.

Highlights

Sexual reproduction is presumed to have arisen in the last common ancestor of eukaryotes[1,2] and subsequently was inherited throughout the eukaryotic domain
To explore the biogeographic diversity of T. pseudonana, we sequenced the whole genomes of isolates collected from the Adriatic Sea and the Atlantic, Indian, and Pacific Oceans, in addition to re-sequencing the original reference isolate CCMP 1335 isolated from the Western Atlantic (Supp. 1, Figs S1, S2)
The R distributions of both H-isolates fit the theoretical model predicated on Hardy-Weinberg equilibrium (HWE), exhibiting the expected 2:1 ratio between the numbers of heterozygous to homozygous non-reference positions (Supp. 5.2, Fig. S7)

Summary

Private SNPsg

Cues[13,14,15] trigger periodic sexual events, which restore cell size (inter alia). A few species, including T. pseudonana[16], are able to escape the fate of mitotic size reduction. Each L-isolate has at least 29 longer SNP deserts, ranging in size from ≈50 to 320 Kb that together span nearly 9% of each genome in noncontiguous blocks across multiple chromosomes This pattern eliminates mitotic forms of recombination as potential mechanisms driving these large-scale loss of heterozygosity (LoH) events[22]. Similar to other L-isolates, it contains almost no homozygous non-reference sites, displays high concordance with L-isolate SNPs and SNP deserts (Figs 2A, S6), and has a low crossover rate (Table 1) It appears that CCMP 1014 breached the presumed ecological niche of T. pseudonana and adapted to the local environment as suggested by its physiological differences from CCMP 133535. Our example of T. pseudonana may be generally applicable to other unicellular eukaryotes with rapid rates of asexual reproduction and potential for long-distance dispersal

Materials and Methods

Author Contributions

Findings

Additional Information