Joint inference of evolutionary transitions to self-fertilization and demographic history using whole-genome sequences
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.
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
Max Planck Institute for Plant Breeding Research (open access funding)
- Stefan Strütt
- Stefan Laurent
No external funding was received for this work.
- Vincent Castric, Université de Lille, France
- Received: August 2, 2022
- Accepted: May 8, 2023
- Accepted Manuscript published: May 11, 2023 (version 1)
© 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.
- Page views
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
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)
- Evolutionary Biology
Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the trait bearer’s cost-benefit difference. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit differences at greater trait magnitudes. Using the cavitation-shooting weapons found in the big claws of male and female snapping shrimp, we test whether size- and sex-dependent expenditures explain scaling and sex differences in weapon size. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest statistical power, smaller individuals showed steeper tradeoffs. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, smaller females exhibited steeper tradeoffs. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mates. In conclusion, we identified size-dependent tradeoffs that could underlie reliable scaling of costly traits. Furthermore, weapons are especially beneficial to males and burdensome to females, which could explain why males have larger weapons than females.
- Evolutionary Biology
The extinct Steller's sea cow (Hydrodamalis gigas; †1768) was a whale-sized marine mammal that manifested profound morphological specializations to exploit the harsh coastal climate of the North Pacific. Yet despite first-hand accounts of their biology, little is known regarding the physiological adjustments underlying their evolution to this environment. Here, the adult-expressed hemoglobin (Hb; a2β/δ2) of this sirenian is shown to harbor a fixed amino acid replacement at an otherwise invariant position (β/δ82Lys→Asn) that alters multiple aspects of Hb function. First, our functional characterization of recombinant sirenian Hb proteins demonstrate that the Hb-O2 affinity of this sub-Arctic species was less affected by temperature than those of living (sub)tropical sea cows. This phenotype presumably safeguarded O2 delivery to cool peripheral tissues and largely arises from a reduced intrinsic temperature sensitivity of the H. gigas protein. Additional experiments on H. gigas β/δ82Asn→Lys mutant Hb further reveal this exchange renders Steller's sea cow Hb unresponsive to the potent intraerythrocytic allosteric effector 2,3-diphosphoglycerate, a radical modification that is the first documented example of this phenotype among mammals. Notably, β/δ82Lys→Asn moreover underlies the secondary evolution of a reduced blood-O2 affinity phenotype that would have promoted heightened tissue and maternal/fetal O2 delivery. This conclusion is bolstered by analyses of two Steller's sea cow prenatal Hb proteins (Hb Gower I; z2e2 and HbF; a2g2) that suggest an exclusive embryonic stage expression pattern, and reveal uncommon replacements in H. gigas HbF (g38Thr→Ile and g101Glu→Asp) that increased Hb-O2 affinity relative to dugong HbF. Finally, the β/δ82Lys→Asn replacement of the adult/fetal protein is shown to increase protein solubility, which may have elevated red blood cell Hb content within both the adult and fetal circulations and contributed to meeting the elevated metabolic (thermoregulatory) requirements and fetal growth rates associated with this species cold adaptation.