Joint inference of evolutionary transitions to self-fertilization and demographic history using whole-genome sequences
Abstract
The evolution from outcrossing to selfing is a transition that occurred recurrently throughout the eukaryote tree of life, in plants, animals, fungi and algae. Despite some short-term advantages, selfing is supposed to be an evolutionary dead-end reproductive strategy on the long-term and its tippy distribution on phylogenies suggests that most selfing species are of recent origin. However, dating such transitions is challenging while it is central for this hypothesis. We build on previous theories to explicit the differential effect of past changes in selfing rate or in population size on the probability of recombination events along the genome. This allows us to develop two methods making use of full genome polymorphism data to 1) test if a transition from outcrossing to selfing occurred, and 2) infer its age. The sequentially Markov coalescent based (teSMC) and the Approximate Bayesian Computation (tsABC) methods use a common framework based on a transition matrix summarizing the distribution of times to the most recent common ancestor along the genome, allowing to estimate changes in the ratio of population recombination and mutation rates in time. We first demonstrate that our methods can disentangle between past change in selfing rate from past changes in demographic history. Second, we assess the accuracy of our methods and show that transitions to selfing as old as approximatively 2.5Ne generations can be identified from polymorphism data. Third, our estimates are robust to the presence of linked negative selection on coding sequences. Finally, as a proof of principle, we apply both methods to three populations from Arabidopsis thaliana, recovering a transition to selfing which occurred approximately 600,000 years ago. Our methods pave the way to study recent transitions to predominant self-fertilization in selfing organisms and to better account for variation in mating systems in demographic inferences.
Data availability
The current manuscript is a computational study, so no data have been generated for this manuscript. Modelling code is available at the following repositories.tsABC: https://github.com/sstruett/tsABCteSMC: https://github.com/TPPSellinger/eSMC2scripts used for the analyses in Strütt and Sellinger et al: https://github.com/laurentlab-mpipz/struett_and_sellinger_et_al
-
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana1001genomes, DOI: 10.1016/j.cell.2016.05.063.
Article and author information
Author details
Funding
Max Planck Institute for Plant Breeding Research (open access funding)
- Stefan Strütt
- Stefan Laurent
No external funding was received for this work.
Copyright
© 2023, Strütt et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,186
- views
-
- 145
- downloads
-
- 10
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Evolutionary Biology
Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ ‘mineralization of extracellular matrix’ attributed to hyaline rotaliid shells, or ‘mineralization within intracellular vesicles’ attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We have found under a high-resolution scanning electron microscopy (SEM) that precipitation of high-Mg calcitic mesocrystals in porcelaneous shells takes place in situ and form a dense, chaotic meshwork of needle-like crystallites. We have not observed calcified needles that already precipitated in the transported vesicles, what challenges the previous model of miliolid mineralization. Hence, Foraminifera probably utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls in both models are therefore most likely created by intravesicular accumulation of pre-formed liquid amorphous mineral phase deposited and crystallized within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well conserved in two clades that represent different chamber formation modes.
-
- Evolutionary Biology
- Genetics and Genomics
The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help to understand the evolution and biology of enigmatic species better. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.