Genomics of plant speciation

Abstract

Studies of plants have been instrumental for revealing how new species originate. For several decades, botanical research has complemented and, in some cases, challenged concepts on speciation developed via the study of other organisms while also revealing additional ways in which species can form. Now, the ability to sequence genomes at an unprecedented pace and scale has allowed biologists to settle decades-long debates and tackle other emerging challenges in speciation research. Here, we review these recent genome-enabled developments in plant speciation. We discuss complications related to identification of reproductive isolation (RI) loci using analyses of the landscape of genomic divergence and highlight the important role that structural variants have in speciation, as increasingly revealed by new sequencing technologies. Further, we review how genomics has advanced what we know of some routes to new species formation, like hybridization or whole-genome duplication, while casting doubt on others, like population bottlenecks and genetic drift. While genomics can fast-track identification of genes and mutations that confer RI, we emphasize that follow-up molecular and field experiments remain critical. Nonetheless, genomics has clarified the outsized role of ancient variants rather than new mutations, particularly early during speciation. We conclude by highlighting promising avenues of future study. These include expanding what we know so far about the role of epigenetic and structural changes during speciation, broadening the scope and taxonomic breadth of plant speciation genomics studies, and synthesizing information from extensive genomic data that have already been generated by the plant speciation community.

Keywords: genomic islands of speciation; hybrid speciation; polyploid speciation; reproductive isolation; standing genetic variation; structural variation.

Figure 1

The genome-wide pattern of sequence differentiation at different stages of speciation (early, mid, late). In the early stages of speciation, RI loci are the only F_ST peaks. As divergence proceeds, other processes (e.g., sorting of ancestral variation, local reductions in Ne, linked selection, etc.) cause additional F_ST peaks. In late speciation, global rises in F_ST further obscure the ability to identify peaks.

Figure 2

The effects of chromosomal translocation on recombination suppression. (A) A reciprocal translocation between two non-homologous chromosomes. (B–D) In different scenarios, recombination rate in heterozygous individuals is reduced (B) only around the translocation breakpoints, (C) around the breakpoint of one chromosome and in the translocated segment of the other chromosome, or (D) around the breakpoint of one chromosome and for the entire chromosome except for the translocated segment on the other. Gray lines represent recombination rate in individuals homozygous for the original karyotype, and blue, green, and orange lines represent recombination rate in heterozygous individuals. The x axes in (B)–(D) are used to indicate position along the original chromosomes. Black circles indicate locations of centromeres, and red triangles indicate locations of the breakpoints on the original chromosomes. Note that recombination is also suppressed around centromeres.

Figure 3

Potential impacts of gene flow (or its absence) on lineage divergence, speciation, or extinction. Gene flow levels are represented by the thickness of the dashed lines, with thicker lines indicative of greater gene flow. In allopatric speciation, diverging lineages (A and B) are isolated because of a physical barrier, represented by a mountain range in the diagram. Biological reproductive barriers are expected to evolve over time, as marked by a red “X.” Speciation in the presence of gene flow depicts gene flow diminishing over time as RI strengthens because of adaptive divergence. In homoploid hybrid speciation, hybrids may form an independent lineage (C) when they become reproductively isolated from parental lineages. This may occur because of ecological divergence and sorting of genetic and chromosomal incompatibilities (or both). However, if hybrids of low fitness are selected against, then prezygotic barriers between parental lineages may be strengthened over time, as indicated by the darkening of the red “X.” Introgression may occur between closely related species (A and C). An increased rate of introgression could lead to extinction through genetic swamping, in which species A becomes indistinguishable phenotypically from species C. This is denoted by C^A.

Figure 4

Successive polyploid speciation events and associated genome size dynamics. The phylogeny on top illustrates a clade that sustained one ancient autopolyploid speciation event (1) and one recent allopolyploid speciation event (2). Occasional extinction events are marked with “X.” Note that, while paleopolyploidy events can be a consequence of either auto- or allopolyploidy, discerning between the two possibilities is often not possible for ancient polyploids. The middle part of the figure traces genome size dynamics for a subset of species in the phylogeny shown in darker red. Advances made possible with the help of genomics data include identification of paleopolyploidization events across land plants, understanding the mechanistic basis of diploidization and long-term polyploid evolution, as well as identifying neopolyploids and studying the early meiotic challenges associated with WGD.

Figure 5

The evolution of a Bateson–Dobzhansky–Muller hybrid incompatibility because of genetic hitchhiking. Results from Wright et al. (2013), focusing on M. guttatus, are used to illustrate this process. (A) An allele at the Tol1 locus that confers copper tolerance (blue circle) has swept to near-fixation (>99% frequency) in a copper mine population in California since the mine’s inception around 150 years ago. A hybrid lethality allele (orange square) at the adjacent Nec1 locus has been swept to high frequency alongside the copper-tolerant allele. (B) The swept allele at Nec1 causes hybrid necrosis in crosses between mine population plants and off-mine populations plants, interacting with several unknown loci to cause necrosis.

Figure 6

Hypothetical scenarios showing the influence of time and geography on introgression, selection on standing variation, and hybrid incompatibilities from de novo mutations. Genetic loci are shapes. Alleles are shades/colors. Each species is shown as a few sample individuals. Each individual is diploid with two copies of each gene. Tightly linked genes are shown close together, far genes are separated by //. The ancestral blue alleles of the star and circle loci are essential or facilitate, respectively, survival at higher elevations. The yellow and red circle alleles are beneficial to low-elevation populations but cannot mix with the blue circle allele, impeding gene flow between high and low species. Introgression introduced the yellow allele to the ancestral population. Elevation is used as a visual example here, but this could equivalently be different niches of any type in the same location or different locations.

Figure 7

Genomics can facilitate the study of speciation that is triggered by genetic drift via phylogenomics and the reconstruction of demography. Two hypothetical scenarios are considered, both of which result in the same contemporary differences in range size and population size among species. Only scenario 1 (left) is consistent with speciation triggered by genetic drift. In this case, two of the three speciation events (i.e., speciation 2 and speciation 3) could have been the direct result of drift-induced genetic changes because the timing of speciation (gray shading) coincides with sharp decreases in effective population size (top panels). Consistent with speciation triggered by genetic drift, the phylogeny on the left also identifies species A and C as paraphyletic.