Breaking the species barrier: recurrent genomic introgressions from very distant lineages in a ciliate

Abstract

The process of speciation, through which two reproductively isolated species emerge from an ancestral population, is often gradual, including a period during which gene flow still occurs, and hence speciation remains reversible. However, if isolation persists, the progressive accumulation of genetic incompatibilities ultimately locks the speciation process, reaching the point where hybrid offspring are inviable or sterile. In plants and animals, the establishment of species barriers is quite rapid: beyond a net genetic divergence of 0.02 substitutions per synonymous site, interspecific introgressions become extremely rare. Here we report that in ciliates, species barriers can be broken despite huge genetic divergence. We show that the genome of Paramecium sonneborni contains hundreds of DNA segments that were acquired by recurrent horizontal transfers from multiple very distant lineages (synonymous divergence [~]1 substitution/site). These segments approach the size of full-length chromosomes, which indicates that they were introgressed by inter-specific mating. These data show that in the ancestry of P. sonneborni, hybridization events with highly divergent species occurred repeatedly and led to viable and fertile offspring. We propose that this unexpected promiscuous sexual behavior is made possible by the fact that paramecia separate somatic and germline functions in two types of nuclei: the elimination of non-self DNA fragments during the development of the somatic genome allows individuals of a species to remain phenotypically the same, despite recurrent genetic flow from distant species into their germline. Significance StatementAn important issue in evolutionary biology is to understand the process of speciation, i.e. how two reproductively isolated species emerge from an ancestral population. Various factors can initiate the speciation process, but whatever the initial factor, once two populations become reproductively isolated, they start accumulating genetic incompatibilities. In plants and animals these incompatibilities accumulate rapidly, preventing the formation of viable and fertile hybrids, except between very closely related species. We show here that this rule does not apply to all eukaryotes. We discovered that the unicellular eukaryote Paramecium sonneborni recurrently acquired large DNA segments via hybridization with very distantly related species. This unexpected phenomenon highlights the diversity of factors that affect the delineation of species across eukaryotes.