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How Reticulated Are Species? Think Again James Mallet1)2)*, Nora Besansky3) and Matthew W

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How Reticulated Are Species? Think Again James Mallet1)2)*, Nora Besansky3) and Matthew W View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by UCL Discovery Insights & Perspectives How reticulated are species? Think again James Mallet1)2)*, Nora Besansky3) and Matthew W. Hahn4) Many groups of closely related species have reticulate phylogenies. Recent well as microbes. Reproductively iso- genomic analyses are showing this in many insects and vertebrates, as well as lated species and bifurcating phyloge- in microbes and plants. In microbes, lateral gene transfer is the dominant nies have become an important basis for process that spoils strictly tree-like phylogenies, but in multicellular eukaryotes our understanding of evolution; now this bedrock seems threatened. As an hybridization and introgression among related species is probably more ideal, species are often taken to be important. Because many species, including the ancestors of ancient major evolutionarily independent populations lineages, seem to evolve rapidly in adaptive radiations, some sexual that are reproductively isolated from compatibility may exist among them. Introgression and reticulation can thereby other such species, for example in the affect all parts of the tree of life, not just the recent species at the tips. Our “biological species concept,” although it was always known that hybridization understanding of adaptive evolution, speciation, phylogenetics, and compar- does occur [15]. Reticulate evolution in ative biology must adapt to these mostly recent findings. Introgression has plants has long been recognized [16], important practical implications as well, not least for the management of but recent genomic evidence from genetically modified organisms in pest and disease control. animals suggest that reticulation might be much more common than antici- Keywords: pated [17, 18]. Given abundant new .admixture; homoplasy; introgression; phylogenetic discordance; speciation; data, it is time to enquire whether a species concepts; tree of life major shift in our understanding of species, speciation, and phylogenetics Introduction tidy tree picture was threatened: is taking place. sequencing of more microbial genes Not so long ago, analysis of microbial and then whole genomes quickly led to 16S ribosomal RNA sequences led to a an understanding of the importance of revolutionary new “Universal Tree of horizontal or lateral gene transfer, the Prokaryotes: Is there a Life,” consisting of three monophyletic incorporation of foreign genes into the universal tree of life? domains, here referred to as the Bacte- genome. Some of the major transitions ria, the Archaea, and the Eukarya or in evolution were clearly due to lateral Tree-like relationships among species eukaryotes [1, 2]. Yet almost as soon as transfer: the eukaryotes were formed by arise because the genome the new system was established, this endosymbiosis of a-proteobacteria with evolves within cells. When a cell Archaea to form the eukaryotes. Later, divides, copies of the same genome DOI 10.1002/bies.201500149 endosymbiosis of cyanobacteria with are found in each daughter cell. Ulti- eukaryotes led to green algae and mately, after populations of organisms plants. Many other gene transfers diverge or “speciate,” evolution along 1) Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, together with multiple other endosym- each branch will leave genomic signals USA bioses have been inferred. Microbiolo- of that branching event in daughter 2) Department of Genetics, Evolution and gists began to argue that the “tree” of lineages. Sex and recombination can Environment, University College London, London, UK life was more like a web or network than obscure this picture, but in both 3) Department of Biological Sciences and Eck a tree [3–5]. Bacteria and Archaea sex (in the Institute for Global Health, University of Notre Today, whole genome sequencing is eukaryote-like sense of homologous Dame, Notre Dame, IN, USA providing unprecedented phylogenetic gene exchange) is mostly a transaction 4) Department of Biology and School of Informatics and Computing, Indiana University, information about whole groups of between closely related individuals, Bloomington, IN, USA eukaryotes [6–14]. Here we review mostly within the same populations or genomic evidence suggesting that retic- “species” [19–22]. Eukaryotes are simi- *Corresponding author: James Mallet ulate evolution may have considerable lar [23, 24]. Lateral transfer involving E-mail: [email protected] impact in multicellular eukaryotes as non-homologous exchange, on the 140 www.bioessays-journal.com Bioessays 38: 140–149, ß 2015 The Authors. BioEssays Published by WILEY Periodicals, Inc. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. .....Insights & Perspectives J. Mallet et al. other hand, will lead to more wide- derided as “the tree of one per pathologies to those found in prokar- ranging phylogenetic discordance. In cent” [32]. Around 80% of eukaryotic yotes. This raises doubt about the prokaryotes, both sex and lateral trans- proteins are actually more closely eukaryotic Tree of Life as a whole. Apart Think again fer involve relatively few genes at a time related to homologs in the Bacteria from phylogenetic estimation error and or even if more extensive, usually much than in the Archaea; the Universal homoplasy, there are three main causes less than 50% of the genome. Neverthe- Tree’scloserarchaeal-eukaryoteaffin- of phylogenetic incongruence: lateral less, multiple exchanges may take ityisreflectedinonlyabout15%of gene transfer, incomplete lineage sort- place, and very large fractions of eukaryote proteins [28, 32], including ing, and introgression. the genome might eventually be those used by Ciccarelli et al. [30]. exchanged with other lineages or spe- Because of concerns such as these, the cies over long periods. If so, it is possible existence of species and of the Univer- Lateral transfer that the signals of the organismic sal Tree in microbes has been dis- genealogy (the original “tree of cells”) missed as a “myth” in the prokaryote In Eukaryotes, lateral or horizontal in the genome will be obliterated by literature [33]. Whether species or the gene transfer is widespread, but is multiple phylogenetic signals from sex Universal Tree exist in prokaryotes has usually thought to be rare compared and lateral transfer. become almost a philosophical rather to that in prokaryotes [8, 36, 37]. It Before assessing new genomic evi- than a biological issue [29], but it does seems to be associated mainly with dence for phylogenetic discordance in seem clear that most of the original single-celled eukaryotes (the “pro- multicellular eukaryotes, it is worth Universal Tree, whether identifiable or tists”), especially those that engulf reviewing the controversy raging about not, is located on the far side of what their food, or in multicellular organ- the microbial “Tree of Life” over the last Woese originally intended by the isms with parasites in close cellular few decades. Carl Woese [25] argued Darwinian Threshold. contact with their hosts. Eukaryotes that in spite of considerable lateral clearly seem to have acquired impor- transfer, there is “a genealogy-defining tant genes via lateral transfer from both core of genes whose common history What causes phylogenetic mitochondrial and chloroplast endo- dates back to the root of the universal symbionts, but transfers also originate tree.” Woese suggested that the acqui- incongruence in from other endosymbionts, parasites, sition of sufficient co-adaptation among eukaryotes? and close associates [35]. Lateral pro- these key genes caused life to reach a cesses in eukaryotes, in contrast to “Darwinian threshold,” which permit- Findings of promiscuous gene exchange other possible causes of reticulation, ted divergence into separate species and among prokaryotes have usually may transfer genes between distantly allowed us to trace the organismal been contrasted with supposedly well- related species, but typically involve history, even while lateral transfer behaved trees in eukaryotes [33, 34]. relatively few genes at a time, as in obscures the universal tree for many Eukaryote genomes originated when an prokaryotes. Lateral transfer is com- other genes. According to Woese, before archaeal cell acquired many bacterial mon in some multicellular groups [36], the Darwinian threshold was reached, genes, in part but certainly not only such as bdelloid rotifers, which, inter- divergence and speciation could not associated with the bacterial endosym- estingly, lack meiotic sex [38, 39]. take place, and no tree of genes would biotic origins of mitochondria and Horizontal gene transfer in the mito- allow us to trace the organismal history. chloroplasts [35]. Eukaryotes also chondrial genomes of plants and yeasts It quickly became apparent that invented meiosis, which allows recom- is also widespread [40]. However, lateral transfer does indeed swamp the bination of whole genomes. In multicel- horizontal transfer is probably not an signal of the Universal Tree in micro- lular eukaryotes, reproduction itself overriding factor in the evolution of the bial genomes: in fact no other genes often involves meiosis. This innovation nuclear protein coding genes of most support Woese’s original 16S RNA effectively destroys the tree-like signal multicellular eukaryotes, unlike those tree [26]. Many
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