In phylogenetics, reconciliation is an approach to connect the history of two or more coevolving biological entities. The general idea of reconciliation is that a phylogenetic tree representing the evolution of an entity (e.g. homologous genes or symbionts) can be drawn within another phylogenetic tree representing an encompassing entity (respectively, species, hosts) to reveal their interdependence and the evolutionary events that have marked their shared history. The development of reconciliation approaches started in the 1980s, mainly to depict the coevolution of a gene and a genome, and of a host and a symbiont, which can be mutualist, commensalist or parasitic. It has also been used for example to detect horizontal gene transfer, or understand the dynamics of genome evolution.
Phylogenetic reconciliation can account for a diversity of interdependent evolutionary trajectories, from molecules to populations and cultures. A recent avatar of the importance of interactions between levels of organization is the holobiont concept, where a macro-organism is seen as a complex partnership of diverse species. Modeling the evolution of complex entities is one of the current foci of research on reconciliation.
Phylogenetic trees as nested structures
Phylogenetic trees are intertwined at all levels of organization, integrating conflicts and dependencies within and between levels. Macro-organism populations migrate between continents, their microbe symbionts switch between populations, the genes of their symbionts transfer between microbe species, and domains are exchanged between genes. This list of organization levels is not representative or exhaustive, but gives a view of levels where reconciliation methods have been used. As a generic method, reconciliation could take into account numerous other levels. For instance, it could consider the syntenic organization of genes, the interacting history of transposable elements and species, the evolution of a protein complex across species. The scale of evolutionary events considered can go from population events such as geographical diversification to nucleotids levels one inside genes,Felsenstein J (2004) Inferring Phylogenies. Oxford University Press including for instance chromosome levels events inside genomes such as whole genome duplication.
Phylogenies have been used for representing the diversification of life at many levels of organization: macro-organisms, their cells throughout development, micro-organisms through marker genes, chromosomes, proteins, protein domains, and can also be helpful to understand the evolution of human culture elements such as languages or fairy tales. At each of these levels, phylogenetic trees describe different stories made of specific diversification events, which may or may not be shared among levels. Yet because they are structurally nested (similar to matryoshka dolls) or functionally dependent, the evolution at a particular level is bound to those at other levels.
Phylogenetic reconciliation is the identification of the links between levels through the comparison of at least two associated trees. Originally developed for two trees, reconciliations for more than two levels have been recently constructed (see section Explicit modeling of three or more levels). As such, reconciliation provides evolutionary scenarios that reveal conflict and cooperation among evolving entities. These links may be unintuitive, for instance, genes present in the same genome may show uncorrelated evolutionary histories while some genes present in the genome of a symbiont may show a strong coevolution signal with the host phylogeny. Hence, reconciliation can be a useful tool to understand the constraints and evolutionary strategies underlying the assemblage that forms a holobiont.
Because all levels essentially deal with the same object, a phylogenetic tree, the same models of reconciliation—in particular those based on duplication-transfer-loss events, which are central to this article—can be transposed, with slight modifications, to any pair of connected levels: an "inner", "lower", or "associate" entity (e.g. gene, symbiont species, population) evolves inside an "upper", or "host" one (respectively species, host, or geographical area). The upper and lower entities are partially bound to the same history, leading to similarities in their phylogenetic trees, but the associations can change over time, become more or less strict or switch to other partners.
History
The principle of phylogenetic reconciliation was introduced in 1979 to account for differences between genes and species-level phylogenies. In a parsimonious setting, two evolutionary events, gene duplication and gene loss were invoked to explain the discrepancies between a gene tree and a species tree. It also described a score on gene trees knowing the species tree and an aligned sequence by using the number of gene duplication, loss, and nucleotide replacement for the evolution of the aligned sequence, an approach still central today with new models of reconciliation and phylogeny inference.
The term reconciliation has been used by Wayne Maddison in 1997,Wayne P. Maddison (1997) Gene Trees in Species Trees, Systematic Biology, 46(3) 523-536. as a reverse concept of "phylogenetic discord" resulting from gene level evolutionary events.
Reconciliation was then developed jointly for the coevolution of host and symbiont and the geographic diversification of species. In both settings, it was important to model a horizontal event that implied parallel branches of the host tree: host switch for host and symbiont and species dispersion from one area to another in biogeography. Unlike for genes and genomes, the coevolution of host and symbiont and the explanation of species diversification by geography are not always the null hypothesis. A visual depiction of the two phylogenies in a tanglegram can help assess such coevolution, although it has no statistical obvious interpretation.
Character methods, such as Brooks Parsimony Analysis, were proposed to test coevolution and reconstruct scenarios of coevolution. In these methods, one of the trees is forgotten except for its leaves, which are then used as a character evolving on the second tree. First models for reconciliation, taking explicitly into account the two topologies and using a mechanistic event-based approach, were proposed for host and symbiont and biogeography. Debates followed, as the methods were not yet completely sound but integrated useful information in a new framework.
Costs for each event and a dynamic programming technique considering all pairs of host and symbiont nodes were then introduced into a host and symbiont approach, both of which still underlie most of the current reconciliation methods for host and symbiont as well as for species and genes.
Reconciliation returned to the framework it was introduced in, gene and species. After character models were considered for horizontal gene transfer, a new reconciliation model, following and improving the dynamic programming approach presented for host and symbiont, effectively introduced horizontal gene transfer to gene and species reconciliation on top of the duplication and loss model.
The progressive development of phylogenetic reconciliation was thus possible through exchanges between multiple research communities studying phylogenies at the host and symbiont, gene and species, or biogeography levels. This story and its modern developments have been reviewed several times, generally focusing on specific pairs of levels, with a few exceptions. New developments start to bring the different frameworks together with new integrative models.
Pocket Gophers and their chewing lices: a classical example
Pocket gophers (Geomyidae) and their chewing lice (Trichodectidae) form a well studied system of host and symbiont coevolution. The phylogeny of host and symbiont and the matching of the leaves of their trees are depicted on the left. For the host, O. stands for Orthogeomys, G. for Geomys and T. for Thomomys; for the symbiont, G. stands for Geomydoecus and T. for Thomoydoecus. Reconciling the two trees means giving a scenario with evolutionary events and matching on the ancestral nodes depicting the coevolution of the two trees. The events considered in this system are the events of the DTL model: duplication, transfer (or host switch), loss, and cospeciation, the null event of coevolution. Two scenarios were proposed in two studies, using two different frameworks which could be deemed as pre-dynamic programming DTLDTL stands for ""Duplication, horizontal Transfer and Loss reconciliation. In modern DTL reconciliation frameworks, costs are assigned to events. The two scenarios were then shown to correspond to maximum parsimonious reconciliation with different cost assignments. The scenario A uses 6 cospeciations, 2 duplications, 3 losses and 2 host switches to reconcile the two trees, while scenario B uses 5 cospeciations, 3 duplications, 3 losses and 2 host switches. The cost of a scenario is the sum of the cost of its events. For instance, with a cost of 0 for cospeciation, 2 for duplication, 1 for loss and 3 for host switch, scenario A has a cost of and scenario B of , and so according to a parsimonious principle, scenario A would be deemed more likely (scenario A stays more likely as long as the cost of cospeciation is less than the cost of duplication).
Development of Phylogenetic Reconciliation Models
Models and methods used today in phylogeny are the result of several decades of research, made progressively complex, driven by the nature of the data and the quest for biological realism on one side, and the limits and progresses of mathematical and algorithmic methods on the other.
Pre-reconciliation models: characters on trees Character methods can be used when there is no tree available for one of the levels, but only values for a character at the leaves of a phylogenetic tree for the other level. A model defines the events of character value change, their rate, probabilities or costs. For instance, the character can be the presence of a host on a symbiont tree, the geographical region on a species tree, the number of genes on a genome tree, or nucleotides in a sequence. Such methods thus aim at reconstructing ancestral characters at internal nodes of the tree.
Although these methods have produced results on genome evolution, the utility of a second tree appears with very simple examples. If a symbiont has recently acquired the ability to spread in a group of species and thus it is present in most of them, character methods will wrongly indicate that the common ancestor of the hosts already had the symbiont. In contrast, a comparison of the symbiont and host trees would show discrepancies revealing horizontal transfers.
The origins of reconciliation: the Duplication Loss model and the Lowest Common Ancestor mapping Duplication and loss were invoked first to explain the presence of multiple copies of a gene in a genome or its absence in certain species. It is possible with those two events to reconcile any two trees, i.e. to map the nodes and branches of the lower and upper trees, or equivalently to give a list of evolutionary events explaining the discrepancies between the upper tree and the lower tree. A most parsimonious Duplication and Loss (DL) reconciliation is computed through the Lowest Common Ancestor (LCA) mapping: proceeding from the leaves to the root, each internal node is mapped to the lowest common ancestor of the mapping of its two children.
A Markovian model for reconciliation