Rapid Speciation Characterized by Incomplete Lineage Sorting in the Globally Distributed Bacterium Sulfitobacter

Abstract

Incomplete lineage sorting (ILS), where ancestral polymorphisms persist through rapid speciation, is a hallmark of eukaryotic radiations but undocumented in prokaryotes. We report ILS associated speciation in the globally distributed marine bacterium Sulfitobacter, analyzing 74 strains from 16 oceanic regions and 15 ecosystem types. Genomic analysis resolved over ten genetically monomorphic clades sharing near uniform whole genome divergence (average nucleotide identity {approx}95%). However, individual genes and even adjacent nucleotide sites support conflicting phylogenetic relationships among clades. The median length of nearly identical sequence blocks supporting alternative topologies is less than 50 base pairs, far shorter than typical adaptive cassettes. This within gene, site level discordance provides a diagnostic signature of ancestral polymorphism retention following rapid fragmentation, ruling out adaptive gene sweeps. Demographic inference places this radiation on a timescale of tens of millennia, 100 to 1,000 fold faster than eukaryotic ILS, and traces the clades to a hyper polymorphic, highly recombining ancestor. Neutral simulations show that transient mutation surges or population bottlenecks alone can generate this pattern, without adaptive selection or ecological partitioning. By bridging eukaryotic and prokaryotic speciation paradigms, our findings demonstrate that ILS, previously considered exclusive to sexual eukaryotes, can drive rapid, neutral diversification in bacteria, expanding the mechanisms known to generate prokaryotic biodiversity.