Speciation: How predictable is genome evolution?
Similar patterns of genomic divergence have been observed in the evolution of plant species separated by oceans.
- Imperial College London, United Kingdom
- Bangor University, United Kingdom
Understanding the formation of new species – a process called speciation – is a central challenge in evolutionary biology and genomics, but many questions remain (Arnegard et al., 2014; Riesch et al., 2017). In particular, are there certain patterns of genome evolution that are repeated? And, if there are, can we predict how genomes will change as new species emerge and diverge?
To date, most studies have focused on the genomes of pairs of closely related species living in close proximity (such as two species of whitefish living in the same set of lakes; Gagnaire et al., 2013), or on the genomes of different lineages within a single species (such as one species of stick insect living on two different host plants; Soria-Carrasco et al., 2014), and have predominantly investigated scenarios where there is some degree of gene flow between the different species or lineages (Wolf and Ellegren, 2017). However, it is thought that most new species emerge in geographically isolated populations and in the absence of gene flow. Now, in eLife, a team of researchers from the United States, China and Canada – including Yibo Dong (North Carolina State University) and Shichao Chen (University of Florida and Tongji University) as joint first authors – report how pairs of closely related flowering plants which live thousands of miles apart genetically diverged during evolution (Dong et al., 2019).
Dong et al. systematically collected and sequenced 20 pairs of closely related species, including 16 pairs that diverged between 2 and 10 million years ago as a result of the Eastern Asian–Eastern North American floristic disjunction (Figure 1). These pairs of species are the ideal system in which to study allopatric speciation (that is, speciation in geographically isolated populations).
Figure 1
Geographical distribution of closely related plant species.
Map showing floristic disjunctions – geographically separated regions than contain closely related plant species: 1) the Eastern Asian–Eastern North American floristic disjunction (blue; Dong et al., 2019); 2) the American Amphitropical floristic disjunction (pink; Raven, 1963); 3) the Madrean–Tethyan floristic disjunction (black; Wen and Ickert-Bond, 2009); 4) the Australia–South America floristic disjunction (green; van den Ende et al., 2017); 5) the Northern–Southern Africa floristic disjunction (yellow; Jürgens, 1997); 6) the disjunction between Linospadix minor in North-East Queensland and L. albertisianus in New Guinea (brown; Osborne et al., 2019).
Image credit: Matthew Coathup.
Dong et al. examined divergence in thousands of genes by measuring the rate at which nucleotide substitutions resulted in a change in the amino acid coded for (Ka), and the rate of nucleotide substitutions that did not result in such a change (Ks). The ratio Ka/Ks is a common index for identifying the selective pressure on a gene: values significantly above one indicate positive selection (i.e. an increase in the frequency of beneficial mutations), and values significantly below one indicate purifying selection (i.e. the removal of deleterious mutations). Despite investigating a diverse range of taxa, Dong et al. found that all species pairs experienced similar patterns of genomic divergence and selection, regardless of their ecologies and morphologies.
In fact, most of the genes measured showed little divergence and, intriguingly, the peak frequencies of Ks, Ka and Ka/Ks for each pair clustered within narrow ranges of small values. This is indicative of a common pattern in the relative numbers of genes at different levels of divergence during allopatric speciation, with only a small number of loci in the genome displaying high levels of divergence. Furthermore, by categorising the Ka/Ks ratios into six groups, Dong et al. found that in all pairs of species the relative number of genes under different selection pressures followed the same order. Moderate purifying selection was most common, followed by strong purifying selection, relaxed purifying selection, weak/moderate positive selection, putatively neutral selection and, finally, strong positive selection. Overall the patterns observed by Dong et al. suggest that it might be possible to make predictions about genome evolution.
While the study focused on the Eastern Asian–Eastern North American floristic disjunction, it is likely that these patterns of genome evolution are a common feature of allopatric speciation. Many other disjunctions exist around the world (Figure 1), and similar analyses of these would determine whether the findings of Dong et al. represent a common rule of genomic divergence. Indeed, recent work by some of the present authors and colleagues has shown that two pairs of palm species – one widely separated, the other not – have values of Ka, Ks and Ka/Ks similar to those reported by Dong et al. (Osborne et al., 2019). This supports the idea that these patterns may be common to genomic divergence in general, regardless of geography.
References
-
Floristic biodiversity and history of African arid regionsBiodiversity and Conservation 6:495–514.https://doi.org/10.1023/a:1018325026863
-
Amphitropical relationships in the floras of North and South AmericaThe Quarterly Review of Biology 38:151–177.https://doi.org/10.1086/403797
-
Transitions between phases of genomic differentiation during stick-insect speciationNature Ecology & Evolution 1:0082.https://doi.org/10.1038/s41559-017-0082
-
Evolution of the Madrean-Tethyan disjunctions and the North and South American amphitropical disjunctions in plantsJournal of Systematics and Evolution 47:331–348.https://doi.org/10.1111/j.1759-6831.2009.00054.x
-
Making sense of genomic islands of differentiation in light of speciationNature Reviews Genetics 18:87–100.https://doi.org/10.1038/nrg.2016.133
Article and author information
Author details
Vincent Savolainen
Publication history
- Version of Record published: September 13, 2019 (version 1)
Copyright
© 2019, Coathup et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,098
- views
-
- 197
- downloads
-
- 0
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Speciation: How predictable is genome evolution?
eLife 8:e50784.
https://doi.org/10.7554/eLife.50784
Further reading
-
- Biochemistry and Chemical Biology
- Evolutionary Biology
The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.
-
- Evolutionary Biology
- Genetics and Genomics
Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.
