Patterns and impacts of nonvertical evolution in eukaryotes: a paradigm shift

Abstract

Evolution of eukaryotic species and their genomes has been traditionally understood as a vertical process in which genetic material is transmitted from parents to offspring along a lineage, and in which genetic exchange is restricted within species boundaries. However, mounting evidence from comparative genomics indicates that this paradigm is often violated. Horizontal gene transfer and mating between diverged lineages blur species boundaries and challenge the reconstruction of evolutionary histories of species and their genomes. Nonvertical evolution might be more restricted in eukaryotes than in prokaryotes, yet it is not negligible and can be common in certain groups. Recognition of such processes brings about the need to incorporate this complexity into our models, as well as to conceptually reframe eukaryotic diversity and evolution. Here, I review the recent work from genomics studies that supports the effects of nonvertical modes of evolution including introgression, hybridization, and horizontal gene transfer in different eukaryotic groups. I then discuss emerging patterns and effects, illustrated by specific examples, that support the conclusion that nonvertical processes are often at the root of important evolutionary transitions and adaptations. I will argue that a paradigm shift is needed to naturally accommodate nonvertical processes in eukaryotic evolution.

Keywords: genetic exchange; horizontal gene transfer; hybridization; introgression; reticulated evolution.

Figure 1

Vertical evolutionary processes leading to gene tree incongruence. Incomplete lineage sorting (top) and duplication followed by differential gene loss (bottom) are vertical evolutionary processes that can result in topologies that are incongruent with the underlying species tree. In incomplete lineage sorting (top), two consecutive speciation events lead to different assortment of alleles present in a population (small colored circles) that can be fixed differentially in the three resulting lineages (top left). As a result, some gene trees (top right) will result in closer relationships for the two most distant lineages of the trio, simply reflecting the histories of the alleles that were fixed in each lineage. In duplication followed by differential gene loss (bottom), an ancestor carries two paralogs resulting from a gene duplication; in subsequent speciations, different paralogs are lost in the different lineages (bottom left), resulting in gene tree topologies that are incongruent with the species tree (bottom right).

Figure 2

Reticulated patterns. Different processes can result in reticulated patterns of evolution. The left panel shows an idealized, fully bifurcating species tree representing the evolutionary relationships among species A to I. Three types of events are marked with circles, ellipses, and arrows: (1) an HGT event from species A to H; (2) a hybridation event between species D and F, originating the hybrid species E; and (3) a hybridization between species H and I resulting in introgression from species H into the genome of species I. The central panels shows gene phylogenies presenting incongruences or altered branch patterns resulting from these events: (1) a gene from species H clusters with homologs from the phylogenetically distant species A and B; (2) conflicting patterns found among gene trees in D and E form a clade to the exclusion of F; in others E and F form a clade to the exclusion of D; and (3) genes from the introgressed regions in species I show shorter distances with homologs of species H (right), as compared with nonintrogressed regions (left). The right panel shows a reticulated tree for the same species, here including information on the past reticulation events.

Figure 3

HGT in multicellular eukaryotes. Examples of multicellular eukaryotes (animals and plants) in which HGTs have been robustly identified (these are mentioned in the main text). Depicted are black bean aphids Aphis fabae (picture by Gaspar Alves), unidentified bdelloid rotifer (picture by Bob Blaylock), the mealybug Planococcus citri (picture by Jeffrey W. Lotz), Amborella trichopoda (picture by Scott Zona), red spider mite Tetranychus urticae (Charles Lam), the moss Physcomitrella patens (Hermann Schachner), the grass Alloteropsis cimicina (J.M. Garg), the fern Polypodium vulgare (André Karwath), and the mouth of a lamprey Petromyzon marinus (public domain). All pictures were taken from wikimedia commons and are shared under the Creative Commons Attribution‐Share Alike 3.0 license (https://creativecommons.org/licenses/by/3.0/), the GNU Free Documentation License, version 1.2 (https://commons.wikimedia.org/wiki/Commons:GNU_Free_Documentation_License,_version_1.2), or the public domain (CC0).

Figure 4

Hybridization at different genetic distances and their possible genomic outcomes. Left panel represents the three possible hybrid zones, as described in Ref. 60. The square indicates a space of connectivity (x‐axis, the amount of gene flow) and genetic relatedness (y‐axis, genetic divergence) between putative lineages. Three different hybrid zones (1, 2, and 3) and a species zone are represented. The species zone corresponds to an area of low genetic divergence and high gene flow between populations. The hybrid zone 1 is defined in an area where either gene flow or genetic relatedness is beyond the boundaries that usually define a species, so that those populations rarely cross and often present some genetic incompatibilities. Hybrid zone 2 corresponds to hybrids between lineages that abruptly separated relatively recently, so that genetic divergence is still low, but the absence of gene flow between the lineages may have resulted in the appearance of incompatibilities. Hybrid zone 3 defines hybrids between very divergent lineages. The right panel depicts typical genomic evolution of the different types of hybrids. Here, the x‐axis represents time (i.e., the amount of generations after the hybridization) and the y‐axis indicates genetic divergence. For simplicity, chromosomes of diploid hybrids with only two homologous chromosomes are represented (center). Hybrids of zone 1 and 2 have initially low sequence divergence (bottom). Given the high gene flow between hybridizing lineages and the ability to backcross with the parentals, hybrids of zone 1 generally result in introgressed genomic regions that are reduced as time progresses. Introgressed regions comprising genes that confer a selective advantage are selectively retained. Given the lack of backcrossing, hybrids of zone 2 evolve as a new lineage and genomes are shaped by chromosomal recombination, leading to the loss of heterozygosity. Hybrids of zone 2 present high divergence among homologous chromosomes from the start (top); they can either evolve through recombination and loss of heterozygosity or, in some circumstances, undergo WGD.