Estimating Species Phylogeny from Gene-Tree Probabilities Despite Incomplete Lineage Sorting: An Example from Melanoplus Grasshoppers

Abstract

Estimating phylogenetic relationships among closely related species can be extremely difficult when there is incongruence among gene trees and between the gene trees and the species tree. Here we show that incorporating a model of the stochastic loss of gene lineages by genetic drift into the phylogenetic estimation procedure can provide a robust estimate of species relationships, despite widespread incomplete sorting of ancestral polymorphism. This approach is applied to a group of montane Melanoplus grasshoppers for which genealogical discordance among loci and incomplete lineage sorting obscures any obvious phylogenetic relationships among species. Unlike traditional treatments where gene trees estimated using standard phylogenetic methods are implicitly equated with the species tree, with the coalescent-based approach the species tree is modeled probabilistically from the estimated gene trees. The estimated species phylogeny (the ESP) is calculated for the grasshoppers from multiple gene trees reconstructed for nuclear loci and a mitochondrial gene. This empirical application is coupled with a simulation study to explore the performance of the coalescent-based approach. Specifically, we test the accuracy of the ESP given the data based on analyses of simulated data matching the multilocus data collected in Melanoplus (i.e., data were simulated for each locus with the same number of base pairs and locus-specific mutational models). The results of the study show that ESPs can be computed using the coalescent-based approach long before reciprocal monophyly has been achieved, and that these statistical estimates are accurate. This contrasts with analyses of the empirical data collected in Melanoplus and simulated data based on concatenation of multiple loci, for which the incomplete lineage sorting of recently diverged species posed significant problems. The strengths and potential challenges associated with incorporating an explicit model of gene-lineage coalescence into the phylogenetic procedure to obtain an ESP, as illustrated by application to Melanoplus, versus concatenation and consensus approaches are discussed. This study represents a fundamental shift in how species relationships are estimated - the relationship between the gene trees and the species phylogeny is modeled probabilistically rather than equating gene trees with a species tree.

Coalescent methods for estimating species trees from phylogenomic data

“…To reduce computational cost, various coalescent-based methods were developed to estimate species trees in two stepsestimating gene trees from multigene sequences and then estimating the species tree from the estimated gene trees. Carstens & Knowles (2007) proposed a coalescent-based approach for estimating species trees from a collection of estimated gene trees. Given the estimated gene trees, this approach calculates the likelihood scores of all possible species trees (Degnan & Salter, 2005).…”

A plastid tree can bring order to the chaotic generic taxonomy of Rytidosperma Steud. s.l. (Poaceae)

“…Explicit methods for deducing species phylogenies from gene trees exist (Lerat et al, 2003;Maddison and Knowles, 2006;Liu et al, 2007;Linnen and Farrell, 2008;Edwards, 2009) but these necessarily rest upon data from entire genomes (Lerat et al, 2003), parts of multiple genomes (e.g. Carstens and Knowles, 2007;Liu et al, 2008;Spinks and Shaffer, 2009) or simulations (e.g. Maddison and Knowles, 2006).…”

Error in Phylogenetic Estimation for Bushes in the Tree of Life

“…The coalescent process, which can lead to discordance between gene trees and species trees, has been extensively studied from both a theoretical [10,[17][18][19] and empirical [20][21][22] standpoint. It is known that there are extreme situations (the "anomaly zone") where the most common gene tree is discordant with the species tree [23].…”