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Both the concept of a Darwinian tree of life (TOL) and the possibility of its accurate reconstruction have been much criticized. Criticisms mostly revolve around the extensive occurrence of lateral gene transfer (LGT), instances of uptake of complete organisms to become organelles (with the associated subsequent gene transfer to the nucleus), as well as the implications of more subtle aspects of the biological species concept. Here we argue that none of these criticisms are sufficient to abandon the valuable TOL concept and the biological realities it captures. Especially important is the need to conceptually distinguish between organismal trees and gene trees, which necessitates incorporating insights of widely occurring LGT into modern evolutionary theory. We demonstrate that all criticisms, while based on important new findings, do not invalidate the TOL. After considering the implications of these new insights, we find that the contours of evolution are best represented by a TOL., (© 2024 The Authors. BioEssays published by Wiley Periodicals LLC.)

Darwinian evolution can be simply stated: natural selection of inherited variations increasing differential reproduction. However, formulated thus, links with biochemistry, cell biology, ecology, and population dynamics remain unclear. To understand interactive contributions of chance and selection, higher levels of biological organization (e.g., endosymbiosis), complexities of competing selection forces, and emerging biological novelties (such as eukaryotes or meiotic sex), we must analyze actual examples. Focusing on mitochondria, I will illuminate how biology makes sense of life's evolution, and the concepts involved. First, looking at the bacterium - mitochondrion transition: merging with an archaeon, it lost its independence, but played a decisive role in eukaryogenesis, as an extremely efficient aerobic ATP generator and internal ROS source. Second, surveying later mitochondrion adaptations and diversifications illustrates concepts such as constructive neutral evolution, dynamic interactions between endosymbionts and hosts, the contingency of life histories, and metabolic reprogramming. Without oxygen, mitochondria disappear; with (intermittent) oxygen diversification occurs in highly complex ways, especially upon (temporary) phototrophic substrate supply. These expositions show the Darwinian model to be a highly fruitful paradigm., (© 2023 The Authors. BioEssays published by Wiley Periodicals LLC.)

Eukaryotic origins are inextricably linked with the arrival of a pre-mitochondrion of alphaproteobacterial-like ancestry. However, the nature of the "host" cell and the mode of entry are subject to heavy debate. It is becoming clear that the mutual adaptation of a relatively simple, archaeal host and the endosymbiont has been the defining influence at the beginning of the eukaryotic lineage; however, many still resist such symbiogenic models. In part 1, it is posited that a symbiotic stage before uptake ("pre-symbiosis") seems essential to allow further metabolic integration of the two partners ending in endosymbiosis. Thus, the author argued against phagocytic mechanisms (in which the bacterium is prey or parasite) as the mode of entry. Such positions are still broadly unpopular. Here it is explained why. Evolutionary thinking, especially in the case of eukaryogenesis, is still dominated by anachronistic reasoning, in which highly derived protozoan organisms are seen as in some way representative of intermediate steps during eukaryotic evolution, hence poisoning the debate. This reasoning reflects a mind-set that ignores that Darwinian evolution is a fundamentally historic process. Numerous examples of this kind of erroneous reasoning are given, and some basic precautions against its use are formulated. Also see the video abstract here https://youtu.be/ekqtNleVJpU., (© 2020 The Authors. BioEssays published by Wiley Periodicals, Inc.)

How did full meiotic eukaryotic sex evolve and what was the immediate advantage allowing it to develop? We propose that the crucial determinant can be found in internal reactive oxygen species (ROS) formation at the start of eukaryotic evolution approximately 2 × 10 9 years ago. The large amount of ROS coming from a bacterial endosymbiont gave rise to DNA damage and vast increases in host genome mutation rates. Eukaryogenesis and chromosome evolution represent adaptations to oxidative stress. The host, an archaeon, most probably already had repair mechanisms based on DNA pairing and recombination, and possibly some kind of primitive cell fusion mechanism. The detrimental effects of internal ROS formation on host genome integrity set the stage allowing evolution of meiotic sex from these humble beginnings. Basic meiotic mechanisms thus probably evolved in response to endogenous ROS production by the 'pre-mitochondrion'. This alternative to mitosis is crucial under novel, ROS-producing stress situations, like extensive motility or phagotrophy in heterotrophs and endosymbiontic photosynthesis in autotrophs. In multicellular eukaryotes with a germline-soma differentiation, meiotic sex with diploid-haploid cycles improved efficient purging of deleterious mutations. Constant pressure of endogenous ROS explains the ubiquitous maintenance of meiotic sex in practically all eukaryotic kingdoms. Here, we discuss the relevant observations underpinning this model., (© 2018 The Authors.)

Background: Recently, important discoveries regarding the archaeon that functioned as the "host" in the merger with a bacterium that led to the eukaryotes, its "complex" nature, and its phylogenetic relationship to eukaryotes, have been reported. Based on these new insights proposals have been put forward to get rid of the three-domain Model of life, and replace it with a two-domain model., Results: We present arguments (both regarding timing, complexity, and chemical nature of specific evolutionary processes, as well as regarding genetic structure) to resist such proposals. The three-domain Model represents an accurate description of the differences at the most fundamental level of living organisms, as the eukaryotic lineage that arose from this unique merging event is distinct from both Archaea and Bacteria in a myriad of crucial ways., Conclusions: We maintain that "a natural system of organisms", as proposed when the three-domain Model of life was introduced, should not be revised when considering the recent discoveries, however exciting they may be.

What kind of symbiosis between archaeon and bacterium gave rise to their eventual merger at the origin of the eukaryotes? I hypothesize that conditions favouring bacterial uptake were based on exchange of intermediate carbohydrate metabolites required by recurring changes in availability and use of the two different terminal electron chain acceptors, the bacterial one being oxygen. Oxygen won, and definitive loss of the archaeal membrane potential allowed permanent establishment of the bacterial partner as the proto-mitochondrion, further metabolic integration and highly efficient ATP production. This represents initial symbiogenesis, when crucial eukaryotic traits arose in response to the archaeon-bacterium merger. The attendant generation of internal reactive oxygen species (ROS) gave rise to a myriad of further eukaryotic adaptations, such as extreme mitochondrial genome reduction, nuclei, peroxisomes and meiotic sex. Eukaryotic origins could have started with shuffling intermediate metabolites as is still essential today., (© 2017 The Authors. BioEssays Published by WILEY Periodicals, Inc.)

Current analysis shows that the last eukaryotic common ancestor (LECA) was capable of full meiotic sex. The original eukaryotic life cycle can probably be described as clonal, interrupted by episodic sex triggered by external or internal stressors. The cycle could have started in a highly flexible form, with the interruption of either diploid or haploid clonal growth determined by stress signals only. Eukaryotic sex most likely evolved in response to a high mutation rate, arising from the uptake of the endosymbiont, as this (proto) mitochondrion generated internal reactive oxygen species. This is consistent with the likely development of full meiotic sex from a diverse set of existing archaeal (the host of the endosymbiont) repair and signalling mechanisms. Meiotic sex could thus have been one of the fruits of symbiogenesis at the basis of eukaryotic origins: a product of the merger by which eukaryotic cells arose. Symbiogenesis also explains the large-scale migration of organellar DNA to the nucleus. I also discuss aspects of uniparental mitochondrial inheritance and mitonuclear interactions in the light of the previous analysis.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'., (© 2016 The Author(s).)

As free-living organisms, alpha-proteobacteria produce reactive oxygen species (ROS) that diffuse into the surroundings; once constrained inside the archaeal ancestor of eukaryotes, however, ROS production presented evolutionary pressures - especially because the alpha-proteobacterial symbiont made more ROS, from a variety of substrates. I previously proposed that ratios of electrons coming from FADH2 and NADH (F/N ratios) correlate with ROS production levels during respiration, glucose breakdown having a much lower F/N ratio than longer fatty acid (FA) breakdown. Evidently, higher endogenous ROS formation did not hinder eukaryotic evolution, so how were its disadvantages mitigated? I propose that the resulting selection pressures favoured the evolution of a variety of eukaryotic 'innovations': peroxisomes for FA breakdown, carnitine shuttles, the linkage of beta-oxidation to antioxidant properties, uncoupling proteins (UCPs) and using mitochondrial uncoupling during beta-oxidation to reduce ROS. Recently observed relationships between peroxisomes and mitochondria further support the model., (© 2014 WILEY Periodicals, Inc.)

Oxygen radical formation in mitochondria is a highly important, but incompletely understood, attribute of eukaryotic cells. I propose a kinetic model in which the ratio between electrons entering the respiratory chain via FADH₂ or NADH is a major determinant in radical formation. During the breakdown of glucose, this ratio is low; during fatty acid breakdown, this ratio is much higher. The longer the fatty acid, the higher the ratio and the higher the level of radical formation. This means that very long chain fatty acids should be broken down without generation of FADH₂ for mitochondria. This is accomplished in peroxisomes, thus explaining their role and evolution. The model explains many recent observations regarding radical formation by the respiratory chain. It also sheds light on the reasons for the lack of neuronal fatty acid (beta-) oxidation and for beneficial aspects of unsaturated fatty acids. Last but not least, it has very important implications for all models describing eukaryotic origins.