Lateral gene transfer from the dead

Abstract

In phylogenetic studies, the evolution of molecular sequences is assumed to have taken place along the phylogeny traced by the ancestors of extant species. In the presence of lateral gene transfer, however, this may not be the case, because the species lineage from which a gene was transferred may have gone extinct or not have been sampled. Because it is not feasible to specify or reconstruct the complete phylogeny of all species, we must describe the evolution of genes outside the represented phylogeny by modeling the speciation dynamics that gave rise to the complete phylogeny. We demonstrate that if the number of sampled species is small compared with the total number of existing species, the overwhelming majority of gene transfers involve speciation to and evolution along extinct or unsampled lineages. We show that the evolution of genes along extinct or unsampled lineages can to good approximation be treated as those of independently evolving lineages described by a few global parameters. Using this result, we derive an algorithm to calculate the probability of a gene tree and recover the maximum-likelihood reconciliation given the phylogeny of the sampled species. Examining 473 near-universal gene families from 36 cyanobacteria, we find that nearly a third of transfer events (28%) appear to have topological signatures of evolution along extinct species, but only approximately 6% of transfers trace their ancestry to before the common ancestor of the sampled cyanobacteria.

Figure 1

Gene trees are the result of the combination of speciation and gene birth and death. As a minimal description we consider: a) that for each of the N species at a rate σ, a speciation occurs, during which the species is succeeded by two descendants, and a random species suffers extinction; b) at a rate δ per gene, a gene duplicates, that is, it is succeeded by two gene copies in the same genome, at a rate τ/(N – 1) per gene per host species, a gene is transferred, resulting in one copy each in the donor and host species, and finally, with a rate λ per gene, a gene is lost. The represented phylogeny c) corresponds to the tree spanned by the n sampled species. A branch of the represented tree corresponds to a series of speciation events, but only the last of these, the speciation event that gives rise to two represented lineages (filled circles, green online) is explicitly present for internal branches as the speciation node terminating the branch. The number of unrepresented species (dashed circles) is always much larger than the number of represented species (full circles).

Figure 2

The overwhelming majority of transfers involve evolution along unrepresented species. A direct transfers (dark gray, blue online) between two terminal branches of the represented phylogeny occurs with rate τ/(N – 1) and involves a single transfer event. An indirect transfer (light gray, red online) that leaves an indistinguishable record in the gene tree topology. To count indirect transfers, we trace their history backwards in time: transfer back to the host branch on the represented tree (branch e) occur with a rate τ/(N– 1) from each of the N – n unrepresented species, of these we are only concerned with ones which descend from the relevant donor branch (branch f), the number of these can be calculated using the exponential coalescence probability and the rate of unrepresented speciations σ/N from the donor branch (branch f).

Figure 3

Reconciling gene trees with the complete phylogeny. a) An evolutionary scenario that involves a transfer event from an unrepresented species. The represented phylogeny is shown as a solid tube with filled circles (green online) corresponding to represented speciations. The unrepresented phylogeny is indicated by dashed tubes, with white circles corresponding to unrepresented speciations (cf. Fig. 1c). The continuous line traces the gene tree spanned by genes in sampled species that is the result of a series of birth and death events along the complete phylogeny; b) a reconciliation of the gene phylogeny from (a), corresponding to the evolutionary scenario depicted in (a). In general, we do not know the evolutionary scenario that has generated the gene phylogeny. However, we can use the dynamic programming algorithm described in the text to calculate the likelihood of the gene tree by summing over all possible reconciliations, that is, all ways to draw the gene tree into the species using speciation, duplication, transfer, and loss events [cf. Eqs. (4)–(7) and Fig. A1] in the Appendix. The likelihood calculation uses the rate of different events (σ, δ, τ, and λ) together with functions describing the extinction (E_e and Ē) and the propagation (G_e and ) of gene linages [cf. Eqs. (A.1)–(A.4)].

Figure 4

LGT events for 36 cyanobacteria. For 473 near universal single-copy families from 36 cyanobacterial genomes gene trees that maximize the joint likelihood were reconstructed. For the trees obtained 1000 reconciliations were sampled. a) The distribution of transfer events (light bars, green online) and the preceding speciation events (dark bars, blue online). The final bin summarizes all events occurring above the root of S. b) The distribution of the time spent by transferred genes evolving along unrepresented species for transfers between overlapping branches (dark bars, red online, 72.2% of transfers) and transfers between nonoverlapping branches (light bars, yellow online, 27.8% of all transfers). Both sets of bins sum to unity. Time units are chosen such that the height of the root of S is 1.0. The age of the root falls in the 3500–2700 My interval (Falcón et al. 2010; Szöllősi et al. 2012). Data are available from Dryad under doi:10.5061/dryad.27d0g.

Figure A1

Diagrams corresponding to reconciliation events. Each diagram corresponds to a term in Equations (4)–(7), with diagrams following each other in the same order as terms in the indicated equation. a) Depicts events that start with a gene lineage u in represented branch e of S at time t +Δt; b) events that start with a gene lineage u in an unrepresented species at time t +Δt; and finally, c) corresponds to represented speciation events in S. To illustrate the correspondence between terms and equations, consider the third diagram in the top row (a) depicting an unrepresented speciation and the corresponding (third) term in Equation (4). This term, , describes the probability that gene lineage u seen at time t +Δt is succeeded as a result of an unrepresented speciation by two gene linages (v and w) one of which (w) is present in the same branch e as u while the other (v) resides in an unrepresented species.