Implications of gene tree heterogeneity on downstream phylogenetic analyses: A case study employing the Fair Proportion index.

Many questions in evolutionary biology require the specification of a phylogeny for downstream phylogenetic analyses. However, with the increasingly widespread availability of genomic data, phylogenetic studies are often confronted with conflicting signal in the form of genomic heterogeneity and incongruence between gene trees and the species tree. This raises the question of determining what data and phylogeny should be used in downstream analyses, and to what extent the choice of phylogeny (e.g., gene trees versus species trees) impacts the analyses and their outcomes. In this paper, we study this question in the realm of phylogenetic diversity indices, which provide ways to prioritize species for conservation based on their relative evolutionary isolation on a phylogeny, and are thus one example of downstream phylogenetic analyses. We use the Fair Proportion (FP) index, also known as the evolutionary distinctiveness score, and explore the variability in species rankings based on gene trees as compared to the species tree for several empirical data sets. Our results indicate that prioritization rankings among species vary greatly depending on the underlying phylogeny, suggesting that the choice of phylogeny is a major influence in assessing phylogenetic diversity in a conservation setting. While we use phylogenetic diversity conservation as an example, we suspect that other types of downstream phylogenetic analyses such as ancestral state reconstruction are similarly affected by genomic heterogeneity and incongruence. Our aim is thus to raise awareness of this issue and inspire new research on which evolutionary information (species trees, gene trees, or a combination of both) should form the basis for analyses in these settings.

Exploring spaces of semi-directed level-1 networks.

Semi-directed phylogenetic networks have recently emerged as a class of phylogenetic networks sitting between rooted (directed) and unrooted (undirected) phylogenetic networks as they contain both directed as well as undirected edges. While various spaces of rooted phylogenetic networks and unrooted phylogenetic networks have been analyzed in recent years and several rearrangement moves to traverse these spaces have been introduced, little is known about spaces of semi-directed phylogenetic networks. Here, we propose a simple rearrangement move for semi-directed phylogenetic networks, called cut edge transfer (CET), and show that the space of semi-directed level-1 networks with precisely k reticulations is connected under CET. This level-1 space is currently the predominantly used search space for most algorithms that reconstruct semi-directed phylogenetic networks. Our results imply that every semi-directed level-1 network with a fixed number of reticulations and leaf set can be reached from any other such network by a sequence of CETs. By introducing two additional moves, R[Formula: see text] and R[Formula: see text], that allow for the addition and deletion, respectively, of a reticulation, we then establish connectedness for the space of all semi-directed level-1 networks on a fixed leaf set. As a byproduct of our results for semi-directed phylogenetic networks, we also show that the space of rooted level-1 networks with a fixed number of reticulations and leaf set is connected under CET, when translated into the rooted setting.

Phylogenetic Diversity Rankings in the Face of Extinctions: The Robustness of the Fair Proportion Index.

Planning for the protection of species often involves difficult choices about which species to prioritize, given constrained resources. One way of prioritizing species is to consider their "evolutionary distinctiveness," (ED) that is, their relative evolutionary isolation on a phylogenetic tree. Several evolutionary isolation metrics or phylogenetic diversity indices have been introduced in the literature, among them the so-called Fair Proportion (FP) index (also known as the ED score). This index apportions the total diversity of a tree among all leaves, thereby providing a simple prioritization criterion for conservation. Here, we focus on the prioritization order obtained from the FP index and analyze the effects of species extinction on this ranking. More precisely, we analyze the extent to which the ranking order may change when some species go extinct and the FP index is recomputed for the remaining taxa. We show that for each phylogenetic tree, there are edge lengths such that the extinction of one leaf per cherry completely reverses the ranking. Moreover, we show that even if only the lowest-ranked species goes extinct, the ranking order may drastically change. We end by analyzing the effects of these two extinction scenarios (extinction of the lowest-ranked species and extinction of one leaf per cherry) for a collection of empirical and simulated trees. In both cases, we can observe significant changes in the prioritization orders, highlighting the empirical relevance of our theoretical findings. [Biodiversity conservation; Fair Proportion index; phylogenetic diversity; species prioritization.].

Effects of discordance between species and gene trees on phylogenetic diversity conservation.

Phylogenetic diversity indices such as the Fair Proportion (FP) index are frequently discussed as prioritization criteria in biodiversity conservation. They rank species according to their contribution to overall diversity by taking into account the unique and shared evolutionary history of each species as indicated by its placement in an underlying phylogenetic tree. Traditionally, phylogenetic trees were inferred from single genes and the resulting gene trees were assumed to be a valid estimate for the species tree, i.e., the "true" evolutionary history of the species under consideration. However, nowadays it is common to sequence whole genomes of hundreds or thousands of genes, and it is often the case that conflicting genealogical histories exist in different genes throughout the genome, resulting in discordance between individual gene trees and the species tree. Here, we analyze the effects of gene and species tree discordance on prioritization decisions based on the FP index. In particular, we consider the ranking order of taxa induced by (i) The FP index on a species tree, and (ii) The expected FP index across all gene tree histories associated with the species tree. On the one hand, we show that for particular tree shapes, the two rankings always coincide. On the other hand, we show that for all leaf numbers greater than or equal to five, there exist species trees for which the two rankings differ. Finally, we illustrate the variability in the rankings obtained from the FP index across different gene tree and species tree estimates for an empirical multilocus mammal data set.

Classes of explicit phylogenetic networks and their biological and mathematical significance.

The evolutionary relationships among organisms have traditionally been represented using rooted phylogenetic trees. However, due to reticulate processes such as hybridization or lateral gene transfer, evolution cannot always be adequately represented by a phylogenetic tree, and rooted phylogenetic networks that describe such complex processes have been introduced as a generalization of rooted phylogenetic trees. In fact, estimating rooted phylogenetic networks from genomic sequence data and analyzing their structural properties is one of the most important tasks in contemporary phylogenetics. Over the last two decades, several subclasses of rooted phylogenetic networks (characterized by certain structural constraints) have been introduced in the literature, either to model specific biological phenomena or to enable tractable mathematical and computational analyses. In the present manuscript, we provide a thorough review of these network classes, as well as provide a biological interpretation of the structural constraints underlying these networks where possible. In addition, we discuss how imposing structural constraints on the network topology can be used to address the scalability and identifiability challenges faced in the estimation of phylogenetic networks from empirical data.

Formal Links between Feature Diversity and Phylogenetic Diversity.

The extent to which phylogenetic diversity (PD) captures feature diversity (FD) is a topical and controversial question in biodiversity conservation. In this short paper, we formalize this question and establish a precise mathematical condition for FD (based on discrete characters) to coincide with PD. In this way, we make explicit the two main reasons why the two diversity measures might disagree for given data; namely, the presence of certain patterns of feature evolution and loss, and using temporal branch lengths for PD in settings that may not be appropriate (e.g., due to rapid evolution of certain features over short periods of time). Our article also explores the relationship between the "Fair Proportion" index of PD and a simple index of FD (both of which correspond to Shapley values in cooperative game theory). In a second mathematical result, we show that the two indices can take identical values for any phylogenetic tree, provided the branch lengths in the tree are chosen appropriately. [Evolutionary distinctiveness; feature diversity; phylogenetic diversity; shapley value.].

Classes of tree-based networks.

Recently, so-called tree-based phylogenetic networks have attracted considerable attention. These networks can be constructed from a phylogenetic tree, called the base tree, by adding additional edges. The primary aim of this study is to provide sufficient criteria for tree-basedness by reducing phylogenetic networks to related graph structures. Even though it is generally known that determining whether a network is tree-based is an NP-complete problem, one of these criteria, namely edge-basedness, can be verified in linear time. Surprisingly, the class of edge-based networks is closely related to a well-known family of graphs, namely, the class of generalized series-parallel graphs, and we explore this relationship in full detail. Additionally, we introduce further classes of tree-based networks and analyze their relationships.

On the minimum value of the Colless index and the bifurcating trees that achieve it.

Measures of tree balance play an important role in the analysis of phylogenetic trees. One of the oldest and most popular indices in this regard is the Colless index for rooted bifurcating trees, introduced by Colless (Syst Zool 31:100-104, 1982). While many of its statistical properties under different probabilistic models for phylogenetic trees have already been established, little is known about its minimum value and the trees that achieve it. In this manuscript, we fill this gap in the literature. To begin with, we derive both recursive and closed expressions for the minimum Colless index of a tree with n leaves. Surprisingly, these expressions show a connection between the minimum Colless index and the so-called Blancmange curve, a fractal curve. We then fully characterize the tree shapes that achieve this minimum value and we introduce both an algorithm to generate them and a recurrence to count them. After focusing on two extremal classes of trees with minimum Colless index (the maximally balanced trees and the greedy from the bottom trees), we conclude by showing that all trees with minimum Colless index also have minimum Sackin index, another popular balance index.

Combinatorial properties of phylogenetic diversity indices.

Phylogenetic diversity indices provide a formal way to apportion 'evolutionary heritage' across species. Two natural diversity indices are Fair Proportion (FP) and Equal Splits (ES). FP is also called 'evolutionary distinctiveness' and, for rooted trees, is identical to the Shapley Value (SV), which arises from cooperative game theory. In this paper, we investigate the extent to which FP and ES can differ, characterise tree shapes on which the indices are identical, and study the equivalence of FP and SV and its implications in more detail. We also define and investigate analogues of these indices on unrooted trees (where SV was originally defined), including an index that is closely related to the Pauplin representation of phylogenetic diversity.

Statistical Inconsistency of Maximum Parsimony for k-Tuple-Site Data.

One of the main aims of phylogenetics is to reconstruct the "Tree of Life." In this respect, different methods and criteria are used to analyze DNA sequences of different species and to compare them in order to derive the evolutionary relationships of these species. Maximum parsimony is one such criterion for tree reconstruction, and it is the one which we will use in this paper. However, it is well known that tree reconstruction methods can lead to wrong relationship estimates. One typical problem of maximum parsimony is long branch attraction, which can lead to statistical inconsistency. In this work, we will consider a blockwise approach to alignment analysis, namely the so-called k-tuple analyses. For four taxa, it has already been shown that k-tuple-based analyses are statistically inconsistent if and only if the standard character-based (site-based) analyses are statistically inconsistent. So, in the four-taxon case, going from individual sites to k-tuples does not lead to any improvement. However, real biological analyses often consider more than only four taxa. Therefore, we analyze the case of five taxa for 2- and 3-tuple-site data and consider alphabets with two and four elements. We show that the equivalence of single-site data and k-tuple-site data then no longer holds. Even so, we can show that maximum parsimony is statistically inconsistent for k-tuple-site data and five taxa.

On the Shapley Value of Unrooted Phylogenetic Trees.

The Shapley value, a solution concept from cooperative game theory, has recently been considered for both unrooted and rooted phylogenetic trees. Here, we focus on the Shapley value of unrooted trees and first revisit the so-called split counts of a phylogenetic tree and the Shapley transformation matrix that allows for the calculation of the Shapley value from the edge lengths of a tree. We show that non-isomorphic trees may have permutation-equivalent Shapley transformation matrices and permutation-equivalent null spaces. This implies that estimating the split counts associated with a tree or the Shapley values of its leaves does not suffice to reconstruct the correct tree topology. We then turn to the use of the Shapley value as a prioritization criterion in biodiversity conservation and compare it to a greedy solution concept. Here, we show that for certain phylogenetic trees, the Shapley value may fail as a prioritization criterion, meaning that the diversity spanned by the top k species (ranked by their Shapley values) cannot approximate the total diversity of all n species.

Phylogenetic diversity and biodiversity indices on phylogenetic networks.

In biodiversity conservation it is often necessary to prioritize the species to conserve. Existing approaches to prioritization, e.g. the Fair Proportion Index and the Shapley Value, are based on phylogenetic trees and rank species according to their contribution to overall phylogenetic diversity. However, in many cases evolution is not treelike and thus, phylogenetic networks have been developed as a generalization of phylogenetic trees, allowing for the representation of non-treelike evolutionary events, such as hybridization. Here, we extend the concepts of phylogenetic diversity and phylogenetic diversity indices from phylogenetic trees to phylogenetic networks. On the one hand, we consider the treelike content of a phylogenetic network, e.g. the (multi)set of phylogenetic trees displayed by a network and the so-called lowest stable ancestor tree associated with it. On the other hand, we derive the phylogenetic diversity of subsets of taxa and biodiversity indices directly from the internal structure of the network. We consider both approaches that are independent of so-called inheritance probabilities as well as approaches that explicitly incorporate these probabilities. Furthermore, we introduce our software package NetDiversity, which is implemented in Perl and allows for the calculation of all generalized measures of phylogenetic diversity and generalized phylogenetic diversity indices established in this note that are independent of inheritance probabilities. We apply our methods to a phylogenetic network representing the evolutionary relationships among swordtails and platyfishes (Xiphophorus: Poeciliidae), a group of species characterized by widespread hybridization.

Comparing the rankings obtained from two biodiversity indices: the Fair Proportion Index and the Shapley Value.

The Shapley Value and the Fair Proportion Index of phylogenetic trees have been frequently discussed as prioritization tools in conservation biology. Both indices rank species according to their contribution to total phylogenetic diversity, allowing for a simple conservation criterion. While both indices have their specific advantages and drawbacks, it has recently been shown that both values are closely related. However, as different authors use different definitions of the Shapley Value, the specific degree of relatedness depends on the specific version of the Shapley Value - it ranges from a high correlation index to equality of the indices. In this note, we first give an overview of the different indices. Then we turn our attention to the mere ranking order provided by either of the indices. We compare the rankings obtained from different versions of the Shapley Value for a phylogenetic tree of European amphibians and illustrate their differences. We then undertake further analyses on simulated data and show that even though the chance of two rankings being exactly identical (when obtained from different versions of the Shapley Value) decreases with an increasing number of taxa, the distance between the two rankings converges to zero, i.e., the rankings are becoming more and more alike. Moreover, we introduce our freely available software package FairShapley, which was implemented in Perl and with which all calculations have been performed.