Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data.

Alexander Nater,Hans Ellegren,Linnéa Smeds,Takeshi Kawakami,Reto Burri

doi:10.1093/sysbio/syv045

Abstract

Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.

Highlights

The application of genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology
We assessed the degree of pairwise allele sharing between the four flycatcher species, which is indicative of the prevalence of incomplete lineage sorting (ILS) and/or interspecific gene flow
Between 3.5 and 5.2 million single-nucleotide polymorphisms (SNPs) were private to a single species, with collared flycatcher showing the highest number of SNPs with private derived variation

Summary

Introduction

The application of genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. This framework usually assumes a strictly bifurcating tree, which requires immediate and complete speciation events, and an instantaneous substitution process, which ignores many populationlevel effects, like gradual allele frequency changes (Felsenstein 1981; Golding and Felsenstein 1990) Such an approach might provide satisfactory results in distantly related taxa, but suffers from a number of issues when dealing with evolutionary relationships at shallow time depths. In such cases, a phylogenetic tree inferred from any given genomic locus (a ‘gene’ tree) might not unequivocally reflect the true order of speciation events (the ‘species’ tree), and inconsistent topologies are often obtained across the genome (Maddison 1997; Nichols 2001; Edwards 2009). If introgression is rare and selection for or against it is absent, the fate of an introgressed lineage is determined by chance alone, which might again produce a large variation in observed local gene trees

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