Widespread Discordance of Gene Trees with Species Tree in Drosophila: Evidence for Incomplete Lineage Sorting

Abstract

The phylogenetic relationship of the now fully sequenced species Drosophila erecta and D. yakuba with respect to the D. melanogaster species complex has been a subject of controversy. All three possible groupings of the species have been reported in the past, though recent multi-gene studies suggest that D. erecta and D. yakuba are sister species. Using the whole genomes of each of these species as well as the four other fully sequenced species in the subgenus Sophophora, we set out to investigate the placement of D. erecta and D. yakuba in the D. melanogaster species group and to understand the cause of the past incongruence. Though we find that the phylogeny grouping D. erecta and D. yakuba together is the best supported, we also find widespread incongruence in nucleotide and amino acid substitutions, insertions and deletions, and gene trees. The time inferred to span the two key speciation events is short enough that under the coalescent model, the incongruence could be the result of incomplete lineage sorting. Consistent with the lineage-sorting hypothesis, substitutions supporting the same tree were spatially clustered. Support for the different trees was found to be linked to recombination such that adjacent genes support the same tree most often in regions of low recombination and substitutions supporting the same tree are most enriched roughly on the same scale as linkage disequilibrium, also consistent with lineage sorting. The incongruence was found to be statistically significant and robust to model and species choice. No systematic biases were found. We conclude that phylogenetic incongruence in the D. melanogaster species complex is the result, at least in part, of incomplete lineage sorting. Incomplete lineage sorting will likely cause phylogenetic incongruence in many comparative genomics datasets. Methods to infer the correct species tree, the history of every base in the genome, and comparative methods that control for and/or utilize this information will be valuable advancements for the field of comparative genomics.

Next-generation hybridization and introgression

“…The greatest theoretical challenge posed by genetic introgression studies is proving that the observed pattern of shared alleles between species is the product of recent introgression, as opposed to noncontemporary process such as ancient introgression or the incomplete lineage sorting of genes after speciation (deep coalescence; Pollard et al, 2006;Willyard et al, 2009), as shown in Figure 1. The genetic signature of incomplete lineage sorting is the same as ancient introgression soon after speciation, so we treat these together, and contrast this with recent introgression (introgression here).…”

“…Empirical evidence is therefore required to infer introgression based on shared alleles between species (Slotte et al, 2008;Du et al, 2009). This is particularly a problem in species with a large effective population size (N e ), where high intraspecific allelic diversity makes inferences of hybridization difficult, or in recently speciating groups where levels of divergence are low (Pollard et al, 2006). This problem is illustrated by population studies in oaks (Quercus).…”

Reconciliation with Non-binary Gene Trees Revisited

“…First, we do not consider incomplete lineage sorting (ILS) events, which may not be rare and hence cannot be ignored in certain circumstances [18,20]. Since the effect of an ILS event on the divergence of gene and species trees is similar to that of a duplication event, the concepts proposed here can easily be extended to take into account ILS.…”

Species Relationships in the Genus <I>Bryodaemon</I> (Coleoptera: Curculionidae)

“…Different topologies for different markers are often the result of ancestral polymorphism, incomplete lineage sorting or events of gene flow that occur during the speciation process (POLLARD et al 2006). Discrepancies between nuclear and mitochondrial DNA surveys may also be related to the higher mutation rate of mtDNA (JOHNSON et al 2003).…”