Models, algorithms, and programs for phylogeny reconciliation

International audienceGene sequences contain a gold mine of phylogenetic information. But unfortunately for taxonomists this information does not only tell the story of the species from which it was collected. Genes have their own complex histories which record speciation events, of course, but also many other events. Among them, gene duplications, transfers and losses are especially important to identify. These events are crucial to account for when reconstructing the history of species, and they play a fundamental role in the evolution of genomes, the diversification of organisms and the emergence of new cellular functions. We review reconciliations between gene and species trees, which are rigorous approaches for identifying duplications, transfers and losses that mark the evolution of a gene family. Existing reconciliation models and algorithms are reviewed and difficulties in modeling gene transfers are discussed. We also compare different reconciliation programs along with their advantages and disadvantages

The inference of gene trees with species trees

Molecular phylogeny has focused mainly on improving models for the reconstruction of gene trees based on sequence alignments. Yet, most phylogeneticists seek to reveal the history of species. Although the histories of genes and species are tightly linked, they are seldom identical, because genes duplicate, are lost or horizontally transferred, and because alleles can co-exist in populations for periods that may span several speciation events. Building models describing the relationship between gene and species trees can thus improve the reconstruction of gene trees when a species tree is known, and vice-versa. Several approaches have been proposed to solve the problem in one direction or the other, but in general neither gene trees nor species trees are known. Only a few studies have attempted to jointly infer gene trees and species trees. In this article we review the various models that have been used to describe the relationship between gene trees and species trees. These models account for gene duplication and loss, transfer or incomplete lineage sorting. Some of them consider several types of events together, but none exists currently that considers the full repertoire of processes that generate gene trees along the species tree. Simulations as well as empirical studies on genomic data show that combining gene tree-species tree models with models of sequence evolution improves gene tree reconstruction. In turn, these better gene trees provide a better basis for studying genome evolution or reconstructing ancestral chromosomes and ancestral gene sequences. We predict that gene tree-species tree methods that can deal with genomic data sets will be instrumental to advancing our understanding of genomic evolution.Comment: Review article in relation to the "Mathematical and Computational Evolutionary Biology" conference, Montpellier, 201

Non-Binary Tree Reconciliation with Endosymbiotic Gene Transfer

Gene transfer between the mitochondrial and nuclear genome of the same species, called endosymbiotic gene transfer (EGT), is a mechanism which has largely shaped gene contents in eukaryotes since a unique ancestral endosymbiotic event know to be at the origin of all mitochondria. The gene tree-species tree reconciliation model has been recently extended to account for EGTs: given a binary gene tree and a binary species tree, the EndoRex software outputs an optimal DLE-Reconciliation, that is an embedding of the gene tree into the species tree inducing a most parsimonious history of Duplications, Losses and EGT events. Here, we provide the first algorithmic study for DLE-Reconciliation in the case of a multifurcated (non-binary) gene tree. We present a general two-steps method: first, ignoring the mitochondrial-nuclear (or 0-1) labeling of leaves, output a binary resolution minimizing the DL-Reconciliation and, for each resolution, assign a known number of 0s and 1s to the leaves in a way minimizing EGT events. While Step 1 corresponds to the well studied non-binary DL-Reconciliation problem, the complexity of the formal label assignment problem related to Step 2 is unknown. Here, we show it is NP-complete even for a single polytomy (non-binary node). We then provide a heuristic which is exact for the unitary cost of operations, and a polynomial-time algorithm for solving a polytomy in the special case where genes are specific to a single genome (mitochondrial or nuclear) in all but one species

Efficient Non-Binary Gene Tree Resolution with Weighted Reconciliation Cost

Polytomies in gene trees are multifurcated nodes corresponding to unresolved parts of the tree, usually due to insufficient differentiation between sequences of homologous gene copies. Apart from gene sequences, other information such as that contained in the species tree can be used to resolve such intricate parts of a gene tree. The problem of resolving a multifurcated tree has been considered by many authors, the objective function often being the number of duplications and losses reflected by the reconciliation of the resolved gene tree with the species tree. Here, we present PolytomySolver, an algorithm accounting for a more general model allowing different costs for duplications and losses per species. The time complexity of this algorithm is linear for the unit cost and is quadratic for the general cost, which outperforms the best known solutions so far by a linear factor. We show on simulated trees that the gain in theoretical complexity has a real practical impact on running times

The origin of the legumes is a complex paleopolyploid phylogenomic tangle closely associated with the cretaceous-paleogene (K-Pg) mass extinction event

This is the final version. Available from Oxford University Press via the DOI in this record. The consequences of the Cretaceous-Paleogene (K-Pg) boundary (KPB) mass extinction for the evolution of plant diversity remain poorly understood, even though evolutionary turnover of plant lineages at the KPB is central to understanding assembly of the Cenozoic biota. The apparent concentration of whole genome duplication (WGD) events around the KPB may have played a role in survival and subsequent diversification of plant lineages. To gain new insights into the origins of Cenozoic biodiversity, we examine the origin and early evolution of the globally diverse legume family (Leguminosae or Fabaceae). Legumes are ecologically (co-)dominant across many vegetation types, and the fossil record suggests that they rose to such prominence after the KPB in parallel with several well-studied animal clades including Placentalia and Neoaves. Furthermore, multiple WGD events are hypothesized to have occurred early in legume evolution. Using a recently inferred phylogenomic framework, we investigate the placement of WGDs during early legume evolution using gene tree reconciliation methods, gene count data and phylogenetic supernetwork reconstruction. Using 20 fossil calibrations we estimate a revised timeline of legume evolution based on 36 nuclear genes selected as informative and evolving in an approximately clock-like fashion. To establish the timing of WGDs we also date duplication nodes in gene trees. Results suggest either a pan-legume WGD event on the stem lineage of the family, or an allopolyploid event involving (some of) the earliest lineages within the crown group, with additional nested WGDs subtending subfamilies Papilionoideae and Detarioideae. Gene tree reconciliation methods that do not account for allopolyploidy may be misleading in inferring an earlier WGD event at the time of divergence of the two parental lineages of the polyploid, suggesting that the allopolyploid scenario is more likely. We show that the crown age of the legumes dates to the Maastrichtian or early Paleocene and that, apart from the Detarioideae WGD, paleopolyploidy occurred close to the KPB. We conclude that the early evolution of the legumes followed a complex history, in which multiple auto- and/or allopolyploidy events coincided with rapid diversification and in association with the mass extinction event at the KPB, ultimately underpinning the evolutionary success of the Leguminosae in the Cenozoic.Swiss National Science FoundationUniversity of ZurichNatural Sciences and Engineering Research Council of CanadaNational Environment Research CouncilFonds de la Recherche Scientifique of Belgiu

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

The unpalatable and warning-patterned butterflies _Heliconius erato_ and _Heliconius melpomene_ provide the best studied example of mutualistic Müllerian mimicry, thought – but rarely demonstrated – to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and this was initially hailed as the most striking known case of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of _H. erato_ and _H. melpomene_, supporting repeated codivergence of mimetic populations. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of _H. erato_ and _H. melpomene_ occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. This evidence supports a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change

The inference of gene trees with species trees.

This article reviews the various models that have been used to describe the relationships between gene trees and species trees. Molecular phylogeny has focused mainly on improving models for the reconstruction of gene trees based on sequence alignments. Yet, most phylogeneticists seek to reveal the history of species. Although the histories of genes and species are tightly linked, they are seldom identical, because genes duplicate, are lost or horizontally transferred, and because alleles can coexist in populations for periods that may span several speciation events. Building models describing the relationship between gene and species trees can thus improve the reconstruction of gene trees when a species tree is known, and vice versa. Several approaches have been proposed to solve the problem in one direction or the other, but in general neither gene trees nor species trees are known. Only a few studies have attempted to jointly infer gene trees and species trees. These models account for gene duplication and loss, transfer or incomplete lineage sorting. Some of them consider several types of events together, but none exists currently that considers the full repertoire of processes that generate gene trees along the species tree. Simulations as well as empirical studies on genomic data show that combining gene tree-species tree models with models of sequence evolution improves gene tree reconstruction. In turn, these better gene trees provide a more reliable basis for studying genome evolution or reconstructing ancestral chromosomes and ancestral gene sequences. We predict that gene tree-species tree methods that can deal with genomic data sets will be instrumental to advancing our understanding of genomic evolution