Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction

Abstract

The phylum Placozoa officially consists of only a single described species, Trichoplax adhaerens, although several lineages can be separated by molecular markers, geographical distributions and environmental demands. The placozoan 16S haplotype H2 (Trichoplax sp. H2) is the most robust and cosmopolitan lineage of placozoans found to date. In this study, its genome was found to be distinct but highly related to the Trichoplax adhaerens reference genome, for remarkably unique reasons. The pattern of variation and allele distribution between the two lineages suggests that both originate from a single interbreeding event in the wild, dating back at least several decades ago, and both seem not to have engaged in sexual reproduction since. We conclude that populations of certain placozoan haplotypes remain stable for long periods without bisexual reproduction. Furthermore, allelic variation within and between the two Trichoplax lineages indicates that successful bisexual reproduction between related placozoan lineages might serve to either counter accumulated negative somatic mutations or to cope with changing environmental conditions. On the other hand, enrichment of neutral or beneficial somatic mutations by vegetative reproduction, combined with rare sexual reproduction, could instantaneously boost genetic variation, generating novel ecotypes and eventually species.

Figure 1

Synteny analyses. The Trichoplax sp. H2 genome shows almost complete synteny to the reference genome, up to the resolution the contiguity of the scaffolds can provide. (a) Syntenic dotplot based on collinear gene pairs between the three largest scaffolds of the reference genome and the genomic scaffolds of Trichoplax sp. H2. (b) Block view of the H2 scaffolds syntenic to scaffold 1 of Trichoplax adhaerens (c) Trichoplax sp. H2 scaffold 4 mapped to Trichoplax adhaerens scaffold 1 showing collinear gene pairs. Scaffolds below 50 kb were excluded in the figures for clarity.

Figure 2

dN/dS distribution of collinear gene pairs between Trichoplax adhaerens and Trichoplax sp. H2. The distribution shows that purifying selection dominates, but some genes show evidence of positive selection. Of the initial ≈9,000 pairs, those were removed that showed either dS = 0, dN = 0, or saturated values of either two (≥2).

Figure 3

Hybrid speciation in Placozoa? (a) Allele distribution between H1 and H2 observed in 30 phased coding sequences (CDS). In 80% of investigated CDS the two haplotypes share at least one allele. (b) Sampling site and year of the two haplotypes. (c,d) Two cases of developmental transcriptional regulators in which both haplotypes share one identical allele and the second allele shows a high deviation that is usually not observed within a species. (c) In the case of the NK6 homeodomain we observed two amino acid substitutions within H2, one within H1 and three between the unshared alleles. Note that between Branchiostoma and human there are zero substitutions and even between the cnidarian Nematostella and human there are only two. (d) Similarly, the placozoan SMAD6 ortholog shows high intraindividual variation but both haplotypes share one allele. Shown are the amino acid substitutions between the shared/unshared alleles. The interrupted grey bar in d indicates that the phasing of the transcript resulted in two phased blocks. H1 = Trichoplax adhaerens, H2 = Trichoplax sp. H2, Bf = Branchiostoma floridae, Hs = Homo sapiens, Nv = Nematostella vectensis.