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Phylogenetic Incongruence Arising from Fragmented Speciation in Enteric Bacteria

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Phylogenetic Incongruence Arising from Fragmented Speciation in Enteric Bacteria Phylogenetic incongruence arising from fragmented speciation in enteric bacteria Adam C. Retchless and Jeffrey G. Lawrence1 Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260 Edited* by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved May 17, 2010 (received for review February 2, 2010) Evolutionary relationships among species are often assumed to be DNA. Similarly, antirecombination driven by sequence divergence fundamentally unambiguous, where genes within a genome are and the mismatch repair system causes hybrid sterility in eukar- thought to evolve in concert and phylogenetic incongruence yotes such as Saccharomyces (5), whereas in prokaryotes it simply between individual orthologs is attributed to idiosyncrasies in their prevents the integration of the particular sequence that has di- evolution. We have identified substantial incongruence between verged from the recipient (6). the phylogenies of orthologous genes in Escherichia, Salmonella, As a result, barriers to recombination in bacteria could be lim- and Citrobacter,orE. coli, E. fergusonii, and E. albertii. The source of ited to specific portions of a genome. Consider a bacterial pop- incongruence was inferred to be recombination, because individual ulation freely recombining at all loci. Subpopulations can develop fl genes support con icting topology more robustly than expected through genetic isolation of only a few loci, driven by ecology or from stochastic sequence homoplasies. Clustering of phylogeneti- sequence divergence (7); such subpopulations—recombining at cally informative sites on the genome indicated that the regions many loci but genetically isolated at other loci—could be numer- of recombination extended over several kilobases. Analysis of phy- ous within a larger population. Consistent with this fragmented logenetically distant taxa resulted in consensus among individual speciation model (8), several multilocus sequence analysis gene phylogenies, suggesting that recombination is not ongoing; (MLSA) studies identified closely related populations that appear instead, conflicting relationships among genes in descendent taxa to be recombining at some loci but remain genetically isolated reflect recombination among their ancestors. Incongruence could at others (9, 10). In addition, a comparison of Escherichia and have resulted from random assortment of ancestral polymorphisms EVOLUTION if species were instantly created from the division of a recombining Salmonella genomes revealed extensive variation in the level of population. However, the estimated branch lengths in alternative sequence divergence (after correcting for position and codon se- phylogenies would require ancestral populations with far more di- lection) across regions of the chromosome, suggesting that many versity than is found in extant populations. Rather, these and pre- regions experienced homogenizing recombination as much as 70 vious data collectively suggest that genome-wide recombination million years after other regions had ceased recombination (11). rates decreased gradually, with variation in rate among loci, lead- Critically, excessively diverged regions were clustered around the ing to pluralistic relationships among their descendent taxa. loci where gene gains or losses distinguish Escherichia from Sal- monella; such adaptive changes in gene inventory could have recombination | species | Tree of Life | population structure | incomplete contributed to ecological differentiation within the recombining lineage sorting ancestral population and been the focus of selection against re- combination. This suggests that interference with recombination t first glance, prokaryotes appear to have simple, well-ordered emerged at different loci at different times, driven by adaptation. Arelationships resulting from asexual reproduction and di- Consistent with this view, population genetic simulations exam- vergence by mutation. However, homologous recombination be- ining the recombination-suppressing role of sequence divergence tween closely related strains can lead to complex, nonclonal do not result in population splitting if given recombination relationships (1). Recombination has implications that are so pro- parameters similar to those observed in E. coli (12, 13), but pop- found that its potential within populations is often taken to be the ulation splitting is observed when using the more restrictive definitive feature of species. Mayr’s biological species concept parameters inferred from Salmonella (14). (BSC) frames species in the context of reproductive barriers If recombination barriers are imparted gradually as pop- whereby only conspecific individuals exchange genes; individuals ulations split, they may not be complete before each descendent that fail to recombine represent different species (2). Despite its population splits again. The stepwise acquisition of genetic iso- formulation for sexual eukaryotes, Dykhuizen and Green (1) pro- lation at different locations around the chromosome would lead posed that the BSC could apply to bacteria; operationally, phy- to differing phylogenies of orthologous genes, resulting in the logenies of orthologous genes would be identical for strains of lack of clear organismal relationships. Alternatively, recombi- different species but demonstrably different for strains within spe- nation could cease for all loci instantly when each population cies due to recombination. Several studies have applied these cri- splits, as suggested for Yersinia pestis (15). In this instant speci- teria to multilocus phylogenetic analysis of prokaryotes, supporting ation model, all recombination events occur before the acqui- the notion that there are distinct groups of organisms experiencing sition of genome-wide genetic isolation. Any phylogenetic recombination within each group but not between them (3). incongruence would result from the partitioning of ancestral Despite these results, the BSC may not be generally applicable variation among descendent lineages, which would confound our to prokaryotes, even for taxa that undergo high rates of re- combination. Whereas eukaryotic recombination occurs genome- wide during meiosis, recombination in prokaryotes involves only Author contributions: A.C.R. and J.G.L. designed research; A.C.R. performed research; A.C.R. a small fragment of DNA being introduced into a cell via trans- and J.G.L. contributed new reagents/analytic tools; A.C.R. and J.G.L. analyzed data; and formation, phage-mediated transduction, or plasmid conjugation. A.C.R. and J.G.L. wrote the paper. In both prokaryotes and eukaryotes, recombinants may be The authors declare no conflict of interest. counter-selected when genomic incompatibilities reduce hybrid *This Direct Submission article had a prearranged editor. fitness. In eukaryotes, this inhibits gene exchange genome-wide 1To whom correspondence should be addressed. E-mail: [email protected]. (4), whereas in prokaryotes, recombination interference affects This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. only that small portion of the genome that carries the incompatible 1073/pnas.1001291107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1001291107 PNAS Early Edition | 1of6 Downloaded by guest on September 28, 2021 ability to discern otherwise robust organismal relationships. Here, accepted) or C. youngae (30% accepted). A similar pattern was we test these models directly. observed for the C. youngae/Salmonella clade (Fig. 2A). In contrast to the divergence of Escherichia, Salmonella, and Results Citrobacter, which have been separated for tens of millions of Phylogenetic Discordance in the Enterobacteriaceae Does Not Reflect years, the three species of Escherichia are likely in the final Ongoing Recombination. To identify taxa with potentially con- throes of genetic isolation. MLSA results (18) are consistent with founded relationships, we looked within the well-characterized very low levels of recombination between otherwise distinct species-rich clade of enteric bacteria. To establish a reference groups of Escherichia with divergence comparable to E. coli and phylogeny, we aligned a core genome containing 1,174 ortholo- E. fergusonii. The vast majority of genes in our analysis also gous open reading frames (ORFs) in each of 17 genomes (Table supports the monophyly of E. coli K12 with E. coli UTI89 (Fig. S1), with <15% of aligned sites having gaps in any genome. A 2C) as well as the monophyly of the Escherichia relative to other Neighbor-Net (16) analysis of the concatenated codon alignment genera; however, the relationships between the three Escherichia of these genes shows conflicting phylogenetic signals among these species remain unclear. The E. coli/E. albertii clade was sup- genomes (Fig. 1). Regions with conflicting signal may reflect the ported by 53% of genes and the alternative E. coli/E. fergusonii incongruent histories among genes due to recombination (17). clade by 44% of genes. Thus, these taxa represent the genesis of Examining each gene independently by maximum likelihood the phylogenetic ambiguity that plagues the relationships of (ML), there is near-universal support for the separation of Escherichia, Salmonella, and Citrobacter. Erwinia, Dickeya, Pectobacterium, Serratia, and Yersinia from These gene-based quartets provided no evidence for recent re- Cronobacter and the other genomes (>99% of those alignments combination between species of different genera, indicating that with a single
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