How reticulated are species?

Abstract

Many groups of closely related species have reticulate phylogenies. Recent genomic analyses are showing this in many insects and vertebrates, as well as in microbes and plants. In microbes, lateral gene transfer is the dominant process that spoils strictly tree-like phylogenies, but in multicellular eukaryotes hybridization and introgression among related species is probably more important. Because many species, including the ancestors of ancient major lineages, seem to evolve rapidly in adaptive radiations, some sexual compatibility may exist among them. Introgression and reticulation can thereby affect all parts of the tree of life, not just the recent species at the tips. Our understanding of adaptive evolution, speciation, phylogenetics, and comparative biology must adapt to these mostly recent findings. Introgression has important practical implications as well, not least for the management of genetically modified organisms in pest and disease control.

Keywords: admixture; homoplasy; introgression; phylogenetic discordance; speciation; species concepts; tree of life.

Figure 1

A: “Whole genome” versus “species” tree topologies of the Anopheles gambiae complex in Africa. B: The tree based on the X chromosome only, showing introgression events and estimated node divergence times. The average phylogeny of the whole genome is distorted by autosomal introgression between A. gambiae + coluzzii and A. arabiensis, but this was prevented on the X chromosome by X‐linked hybrid incompatibilities and multiple overlapping inversions that prevent recombination. Modified and reprinted from 18 with permission from AAAS.

Figure 2

Phylogenetic discordance B/D mimicry region of Heliconius genomes. A: F _ST plot shows divergent optix regulatory region determining mimicry differences between geographic races within H. melpomene. Mimicry has been shown to have very strong adaptive value in Heliconius. B: The same region shows a strong excess of ABBA phylogenetic sites over BABA sites, implicating introgression between H. melpomene and H. timareta. C: Furthermore, the non‐sister species H. elevatus shows a phylogenetic topology indicating introgression of the rayed mimicry pattern from the melpomene‐timareta clade in the same genomic region. Modified and reprinted with permission from 17.

Figure 3

A simple case where introgression can distort the history of species and speciation. By “the true phylogeny,” in this paper, we mean the totality of true histories of every part of the genome. This is not readily depicted: our simplified cartoon of the true phylogeny network above indicates abundant introgression between species 1 and 2 after their bifurcation, but little between sister species 2 and 3. It does not, however, show which gene travels in which direction and when, all of which is surely important information about the “true phylogeny” as well. If introgression is extensive, the whole genome tree (bottom left) may indicate an incorrect bifurcation history, as well as ancestral species that never existed (such as the apparent ancestor of 1 and 2 in the diagram). The true bifurcation history of species is shown bottom right.