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Philosophical Transactions Of The Royal Society Of London. Series B, Biological Sciences[JOURNAL]
Philosophical Transactions Of The Royal Society Of London. Series B, Biological Sciences[JOURNAL]
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200 papers
Asymmetrical social copying drives behavioural cascades following a shock event.
Moussaid M, Toyokawa W, Kurvers R
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987726 · Publisher ↗
When facing disruptive events, such as epidemics, terrorist attacks or financial crises, individuals often exhibit protective behaviours, including mass escape movements and stockpiling essential goods. These collective...
When facing disruptive events, such as epidemics, terrorist attacks or financial crises, individuals often exhibit protective behaviours, including mass escape movements and stockpiling essential goods. These collective responses are predominantly driven by a social amplification process, where an initial decision-maker is imitated by others, triggering large-scale behavioural cascades. However, the mechanisms shaping this phenomenon remain unclear. Here, we present an experiment examining the propagation of protective behaviours in dyadic transmissions involving 210 participants. Our research uncovers an asymmetric social response, where individuals tend to copy protective behaviours more strongly than inaction. This pattern causes large amplification cascades in simulated transmission chains and is more pronounced following a brief but intense shock compared to a longer, minor one. Furthermore, our results demonstrate an extended period of collective vigilance post-shock, suggesting that social transmission can facilitate rapid behavioural adjustment during crises. By examining the interplay between individual protective behaviours and group dynamics, our study contributes to a better understanding of how adaptive social responses emerge in uncertain and dynamic environments. This article is part of the theme issue 'The evolution of collective intelligence'.
Heterogeneous learning strategies interact with social network structure and problem complexity to benefit collective search.
Pykälä M, Dillion D, Galesic M
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987725 · Publisher ↗
Groups can outperform individuals by sharing and aggregating information through diverse social structures and learning strategies that shape how innovations are discovered and transmitted. At the same time, groups must...
Groups can outperform individuals by sharing and aggregating information through diverse social structures and learning strategies that shape how innovations are discovered and transmitted. At the same time, groups must solve problems that vary in complexity, from relatively simple decisions to complex tasks with many interacting components such as scientific discovery. Interdisciplinary research shows that collective outcomes depend on learning strategies, group structure and problem complexity, yet it remains unclear how these factors together influence the success of collective search and problem-solving. We develop an evolutionary agent-based model in which selection operates at the group level: networks compete based on collective performance and reproduce, selecting for successful proportions of learning strategies. We use this framework to study the co-emergence of learning strategies across network sizes and densities and across tasks of varying complexity. Our results show that payoff-biased and frequency-biased social learning can co-exist, with their relative prevalence shifting as a function of network structure and task complexity. These findings suggest that no single learning strategy distribution is universally the best; instead, network structure and task complexity jointly shape the proportions of different learning strategies to support collective search. This article is part of the theme issue 'The evolution of collective intelligence'.
Social structure shapes consensus decision-making norms in small-scale societies.
Vadavalli BD, Garfield ZH, Glowacki L
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987724 · Publisher ↗
Humans are uniquely capable of reaching consensus within large, hierarchically structured societies. Yet the pathways by which consensus emerges, especially under constraints imposed by social organization, remain poorly...
Humans are uniquely capable of reaching consensus within large, hierarchically structured societies. Yet the pathways by which consensus emerges, especially under constraints imposed by social organization, remain poorly understood. We use an agent-based model to explore how marriage structure, social group nesting and decision-making norms can shape a group's ability to reach consensus. In our model, simulated agents are embedded in multi-level social networks and possess noisy information. Decisions are spread via three different cascades, each with different interaction norms. We find that grouping of individuals into families via marriages impedes consensus by slowing the rate of information diffusion and elevating informational entropy, especially when nested further into kin groups. By contrast, increasing the size of nested subgroups in a multi-level network reduces redundant social ties and promotes consensus. Finally, decision-making norms that rely on formation of coalitions or representative bodies lead to faster group decisions by bypassing early-stage clustering of information within families. These results offer insights into how consensus dynamics are shaped by social structure and provide a theoretical bridge between research on network topology, collective intelligence and human social evolution. This article is part of the theme issue 'The evolution of collective intelligence'.
Scaffolding minds: human collective intelligence through space, body and material symbols.
d'Errico F, Meneganzin A, Colagè I
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987723 · Publisher ↗
Human collective intelligence (CI)-the capacity of groups to solve problems, make decisions and acquire knowledge beyond individual capabilities-is here understood as an emergent phenomenon that evolved in our lineage fr...
Human collective intelligence (CI)-the capacity of groups to solve problems, make decisions and acquire knowledge beyond individual capabilities-is here understood as an emergent phenomenon that evolved in our lineage from a distinct trajectory of epistemic niche construction (ENC), and progressively sustained the latter. Humans systematically alter their informational landscapes in materially visible ways by creating enduring spatial and artefactual scaffolds for improved cognitive performance and social coordination. In this paper, we propose a set of criteria to define ENC and track its emergence in the archaeological record. These criteria highlight the importance of persistent, publicly accessible and evolutionarily incremental modifications that sustained behavioural coordination among individuals in space and time. We apply this framework to three major domains of material culture: the structuring of space for collective action, the culturalization of the human body and the emergence of exosomatic artefacts to store coded information. We argue that these practices did not merely externalize knowledge but progressively transformed material culture and environments into targeted epistemic infrastructures able to scaffold and amplify group-level performances characteristic of CI, thus shedding light on the evolution of human cognition and social organization. This article is part of the theme issue 'The evolution of collective intelligence'.
Collaborative reasoning and problem-solving in early childhood.
Köymen B, Waddington O
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987722 · Publisher ↗
A core aspect of human intelligence is the ability to reason. Recently, the social dimension of reasoning has been emphasized such that reasoning enables people to justify their beliefs/proposals to collectively solve pr...
A core aspect of human intelligence is the ability to reason. Recently, the social dimension of reasoning has been emphasized such that reasoning enables people to justify their beliefs/proposals to collectively solve problems, in which the goal of the participants is to reach the decision that provides most benefit to all. An important debate in the literature is whether collaborative reasoning leads to good/optimal decisions. Here, we contrast these traditional and social views on reasoning and review the evidence on whether individuals benefit from collective reasoning in a special population: young children. We argue that collaborative problem-solving contexts uniquely facilitate the development of young children's reasoning as it pushes them to treat their partners' perspectives as equal to their own, enabling them to better understand and evaluate them. This article is part of the theme issue 'The evolution of collective intelligence'.
Ultimate and proximate explanations for human cumulative culture and collective intelligence.
Vinicius L, Gunasekaram C, Migliano AB
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987721 · Publisher ↗
The controversy remains over whether chimpanzee culture is cumulative or why it may have remained incipient compared with human cumulative culture. In this perspective, we argue that many debates over cumulative culture...
The controversy remains over whether chimpanzee culture is cumulative or why it may have remained incipient compared with human cumulative culture. In this perspective, we argue that many debates over cumulative culture and collective intelligence can be clarified by extending the parallels between genetic and cultural evolution. Inspired by Dobzhansky's formulation, we first argue that understanding cultural and cognitive differences between humans and chimpanzees requires evidence from the population-level distribution of evolved cultural traits, in addition to evidence for cultural reinvention or social learning at the individual level. Second, we propose that debates over the role of collective intelligence in cultural evolution can be solved if more attention is given to Tinbergen's differentiation between proximate and ultimate levels of explanation. Since cumulative cultural evolution implies that individuals become less likely to hold the totality of culture even with the assistance of social learning, we propose that hominin intelligence evolved to become at the same time more general, cultural and collective than in other African apes. Finally, we discuss our Foraging Niche Hypothesis, which points to increased fitness returns to tool making and spatial mobility as ultimate explanations, with the later evolution of increased general intelligence offering a proximate account for the cultural divergence between hominins and chimpanzees. This article is part of the theme issue 'The evolution of collective intelligence'.
Cooperative sustainability: a case for collective intelligence.
Koomen R
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987720 · Publisher ↗
Group-dwelling species face challenges that can be overcome with collective intelligence (CI): problem-solving abilities of collectives that outpace those of individuals. The breadth of topics within CI is large and grow...
Group-dwelling species face challenges that can be overcome with collective intelligence (CI): problem-solving abilities of collectives that outpace those of individuals. The breadth of topics within CI is large and growing-simultaneously a strength and a limitation of the field. This article explores a methodological approach for mitigating these limitations by examining variability across species, strategy types and cognitive abilities within the same challenging context: common-pool resource (CPR) dilemmas. In doing so, I formulate a framework for categorizing the breadth of strategies for overcoming CPR dilemmas based on their social cognitive demands. Broadly, these strategies can be grouped into ecological sustainability mechanisms and cooperative sustainability strategies (CSS), ranging from bats sustaining their food supply via diminishing returns of overconsumption to the human practice of developing rules and institutions to manage resources sustainably. I then outline existing connections between CSS and CI, highlight key points of synthesis and discuss how integrating these two fields could generate new research avenues. This article is part of the theme issue 'The evolution of collective intelligence'.
Chimpanzees spontaneously prepare for mutually exclusive possibilities, and collective context strengthens this behaviour.
Warren E, Pilgrim C, Aellen M … +5 more , Morford J, Herrmann E, Mann RP, Biro D, Krupenye C
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987719 · Publisher ↗
In both humans and non-human animals, collectives can sometimes overcome individual cognitive biases or shortcomings to execute more rational behaviour than individuals. To investigate differences in strategy and outcome...
In both humans and non-human animals, collectives can sometimes overcome individual cognitive biases or shortcomings to execute more rational behaviour than individuals. To investigate differences in strategy and outcome between individuals and collectives in a logical reasoning task, we presented an inverted U-shaped tube to individuals and pairs of chimpanzees (Pan troglodytes) and examined their preparatory actions towards rewards that could fall from either end of the tube. Given that individual chimpanzees have typically produced a suboptimal one-handed strategy in past variants of this task, we predicted that pairs would outperform individuals primarily through subjects sharing the apparatus, each placing one hand under one tube end such that they collectively account for both possible outcomes. Unexpectedly, over half of our chimpanzees spontaneously produced the optimal two-handed behaviour (covering both ends) on their own, providing evidence that individuals may be able to reason about mutually exclusive future possibilities. This reduced the capacity for pairs to improve upon individual performance. Notably, however, we observed an increase in individual usage of the two-handed strategy in the collective setting. This individual improvement may have arisen from an effect of collective facilitation, such as competition, suggesting an alternative mechanism through which collectives may outperform individuals. This article is part of the theme issue 'The evolution of collective intelligence'.
Social structure as a form of collective intelligence: a new framework.
Brooker JS, van Leeuwen EJC, Clay Z
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987718 · Publisher ↗
Collective intelligence arises when group-level cognition exceeds the capabilities of individual members, enabling more effective learning, decision-making and problem-solving. While sociality underpins collective behavi...
Collective intelligence arises when group-level cognition exceeds the capabilities of individual members, enabling more effective learning, decision-making and problem-solving. While sociality underpins collective behaviour across taxa, the structural dimensions of social organization remain underexamined as active components of this phenomenon. Here, we propose that social structure-the patterned distribution of relationships and interactions within a group-is not only a context in which cognition unfolds, but also a core mechanism through which collective intelligence is enabled and sustained. Specifically, we argue that social structure emerges from cognition at the individual level, while simultaneously shaping cognition by influencing how information is distributed and applied across the group. Empirical evidence suggests that variations in network connectivity, stability and cohesion in social animals mediate problem-solving at the individual and collective levels. By examining these dynamics, we may come to understand how individuals engage in heuristic and rational decision-making and how social structures support or hinder collective cognition. Our framework situates social structure at the centre of collective cognition, offering a unified model that links individual decision-making with emergent group behaviour. This perspective expands current approaches to distributed cognition and sheds light on the organizational foundations of intelligence across diverse taxa. This article is part of the theme issue 'The evolution of collective intelligence'.
Individual versus collective associative learning in ants.
Gildea M, Kissai A, Gutierrez B … +3 more , Usui A, Sanabria F, Sasaki T
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987717 · Publisher ↗
Although associative learning has been traditionally studied at the individual level, it may also operate in group contexts, particularly in social species such as ants. This study investigated whether colonies of Temnot...
Although associative learning has been traditionally studied at the individual level, it may also operate in group contexts, particularly in social species such as ants. This study investigated whether colonies of Temnothorax rugatulus ants exhibit collective learning-defined as group-level information acquisition emerging from dynamic individual learning-by examining whether individuals learn more effectively in a colony than alone. Using a visual associative learning paradigm, we trained ants to associate a visual cue with food availability and compared performance between isolated individuals and colonies. We tested subjects across 17 sessions, comprising acquisition and reversal phases, and quantified performance based on the time spent at correct versus incorrect cues. Our results revealed that ants trained in colonies learnt associations more rapidly than those trained alone during both phases. Additionally, observations showed that colony-trained ants spent more time in correct corridors during training and engaged in more tandem runs early in learning. These findings suggest that social interactions-particularly recruitment behaviour-enhance associative learning of individual ants in colonies. This study underscores the importance of considering the social environment in learning research and suggests that collective learning may be an adaptive mechanism in social animals. This article is part of the theme issue 'The evolution of collective intelligence'.
Clever vermin? Collective intelligence in rats and roaches.
Rawlings B, Vale GL, Legare C … +3 more , Monfils MH, Proctor DP, Brosnan SF
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41987716 · Publisher ↗
Collective intelligence (CI) is the capacity of groups to outperform individuals in tasks such as decision-making, coordination and problem-solving. A significant challenge to studying CI is that it encompasses a wide va...
Collective intelligence (CI) is the capacity of groups to outperform individuals in tasks such as decision-making, coordination and problem-solving. A significant challenge to studying CI is that it encompasses a wide variety of behaviours that are underpinned by different mechanisms. To balance inclusivity with conceptual clarity, we propose a typology of CI mechanisms including self-organized coordination, distributed decision-making, cooperative problem-solving, statistical aggregation and culture and cultural improvement. This typology helps clarify the minimum requirements for CI and how other, more cognitive complex mechanisms may have layered on top of these. As model comparative species, we focus on two ecologically successful generalists, rats (Rattus) and cockroaches (Blattodea). Cockroaches show evidence of collective behaviours, but these rely on a more ancestral set of mechanisms that lack cognitive complexity. Conversely, rats share important ecological traits with cockroaches but exhibit social traits found in primates, including cultural learning, distributed decision-making, empathy and cooperation. This comparison can show how similar collective outcomes can emerge even with disparate mechanisms and provide a way to uncover evolutionary design principles of CI. Ultimately, we can use such comparisons to determine which features of CI are universal properties of collectives and which are contingent on specific cognitive adaptations. This article is part of the theme issue 'The evolution of collective intelligence'.
Correction: 'The evolutionary puzzle of cognition: challenges and insights from individual-based studies' (2024), by Sol et al.
Sol D, Bateman-Neubert A, Noguer L … +1 more , Taylor AH
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923610 · Publisher ↗
Abstract loading — click title to view on PubMed.
The risk of sexual reproduction promotes the evolution of regulation between host and symbionts.
Zania A, Hogeweg P, von der Dunk S
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923609 · Publisher ↗
Sexual reproduction is a widely spread feature of eukaryotes and was already present in the last eukaryotic common ancestor. While most extant eukaryotes inherit mitochondria from a single parent, the mechanisms enforcin...
Sexual reproduction is a widely spread feature of eukaryotes and was already present in the last eukaryotic common ancestor. While most extant eukaryotes inherit mitochondria from a single parent, the mechanisms enforcing uniparental inheritance vary widely. The first eukaryotes likely would not have evolved such mechanisms yet, so cellular fusion would have led to mitochondrial mixing (biparental inheritance). Here, we explore the evolutionary consequences of biparental inheritance of endosymbionts during host-symbiont coevolution using a multi-level, individual-based model of endosymbiosis. Our results show that biparental inheritance introduces evolutionary conflict, as it facilitates the spread of fast-replicating symbionts, which can drive host populations to extinction. However, in a diverse environment, proto-eukaryotes diversify and adapt to distinct niches, protecting the population from total collapse caused by selfish symbionts. Moreover, this conflict can be resolved through the evolution of signalling mechanisms that allow hosts to regulate symbiont cell cycles. In many cases, sexually reproducing populations not only survive but also outperform their asexual counterparts. We conclude that sexual reproduction could have appeared early during eukaryogenesis and may have facilitated the evolution of host control over the endosymbiont cell cycle. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
Extreme mitochondrial genome complexity in the calcaronean sponge Sycon ciliatum (Fabricius, 1780): fragmentation, gene duplication and mRNA editing.
Lavrov DV, Gettle N
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923608 · Publisher ↗
Mitochondrial genomes (mt-genomes) of calcaronean sponges are among the most unusual in Metazoa. They are fragmented into multiple linear chromosomes (mt-chromosomes) and often rely on insertional mRNA editing to generat...
Mitochondrial genomes (mt-genomes) of calcaronean sponges are among the most unusual in Metazoa. They are fragmented into multiple linear chromosomes (mt-chromosomes) and often rely on insertional mRNA editing to generate functional transcripts. These unusual features have precluded complete characterization of calcaronean mt-genomes using short-read sequencing technologies. Here, we assembled and analyzed the mt-genome of Sycon ciliatum (Fabricius, 1780) using HiFi PacBio data generated by the Aquatic Symbiosis Genomics Project. The mt-genome comprised several megabases of sequence distributed across thousands of chromosomes. While most protein-coding genes were preset in multiple copies, three typical animal mitochondrial protein-coding genes (atp8, nad4L and nad6) and multiple tRNA isotypes were not detected, and only short fragments of mt-rRNA genes were identified. We confirmed that mitochondrial mRNA editing in S. ciliatum occurred through single or double uridine insertions at 200+ sites, and that editing patterns were largely predictable from primary sequence motifs. Unexpectedly, editing sites varied among gene copies and were frequently disrupted by point mutations, leading to substantial changes in encoded amino acid sequences. Most mt-chromosomes were associated with repetitive elements that may function in genome maintenance and recombination. Together, our results reveal a distinctive mode of mt-genome evolution and function, shaped by extreme genome fragmentation, extensive gene duplication and pervasive RNA editing. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
Mitonuclear dynamics in unisexual vertebrates.
Klabacka RL, Hill GE, Dowling DK … +4 more , Sharbrough J, Denton RD, Hall JM, Havird JC
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923607 · Publisher ↗
Sex and mitochondria are inextricably linked in the eukaryotic tree of life, a confounding situation given the uniparental inheritance of mitochondria and the biparental inheritance that sexual reproduction entails. Unis...
Sex and mitochondria are inextricably linked in the eukaryotic tree of life, a confounding situation given the uniparental inheritance of mitochondria and the biparental inheritance that sexual reproduction entails. Unisexual vertebrate lineages, which arise via hybridization and asexually pass on their genetic material to clonal descendants, provide a unique opportunity to study mitochondrial evolution without potentially confounding effects of sex. Hybridity and clonality set unisexual vertebrates apart from other vertebrates and establish a distinct genetic environment that shapes their evolution, especially dynamics between mitochondrial and nuclear genomes. Here, we provide a perspective on the mitonuclear genomic interactions experienced by unisexual vertebrates and the implications of these interactions on mitochondrial function and integration into organismal performance and fitness. Building upon the hypothesis that sexual reproduction arose to maintain coadaptation between co-functioning nuclear and mitochondrial genes, we propose that unisexual vertebrates may be confined to predominantly 'young' lineages because mitonuclear incompatibilities-arising from either hybridity or clonality-increase the probability of extinction over time (the Mitonuclear Erosion Hypothesis). We provide a multidisciplinary collection of strategies to disentangle the effects of clonality and hybridity and quantify the relative degree to which these characteristics contribute to differences in mitochondrial function, organismal performance and fitness. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
The cell nucleus as a barrier against horizontal gene transfer in microbial endosymbioses.
Zachar I, Máté J, Oszoli I
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923606 · Publisher ↗
The origin of eukaryotic cells remains a highly contested problem. While eukaryotes arose from the merger of a bacterial and an archaeal partner giving rise to mitochondria and the cell proper, the order of steps is not...
The origin of eukaryotic cells remains a highly contested problem. While eukaryotes arose from the merger of a bacterial and an archaeal partner giving rise to mitochondria and the cell proper, the order of steps is not known, nor is it understood why it was a singular event. Prokaryotes engage in various cooperative interactions everywhere, yet there is no evidence that they could establish stable endosymbiotic relationships on their own. Many assume that mitochondria came first, and their critical presence and features enabled the complex cellular architecture, including the nucleus. Here we find support for the alternative, claiming that a nuclear compartment was a prerequisite for successful stable endosymbiosis. We review independent lines of evidence suggesting that the pre-existence of a nuclear membrane or equivalent mechanism to separate translation from transcription may have been essential to limit genetic inference owing to extensive horizontal gene transfer in the wake of pre-mitochondrial (endo)symbionts and to stabilize the host genome against foreign DNA, especially from (endo)symbiotic partners. We claim that an asymmetry in control potential between partners is required for successful integration of an endosymbiont. This would explain why there are no further prokaryotic endosymbioses known to us (extant or extinct). We propose predictions that can be tested to support the hypothesis. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
Sensitivity of genome-wide tests for mitonuclear genetic incompatibilities.
Kuster SA, Schumer M, Havird J … +1 more , Sloan DB
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923605 · Full text
Mismatches between interacting mitochondrial and nuclear gene products in hybrids have been proposed to disproportionately contribute to early species boundaries. Under this model, genetic incompatibilities emerge when m...
Mismatches between interacting mitochondrial and nuclear gene products in hybrids have been proposed to disproportionately contribute to early species boundaries. Under this model, genetic incompatibilities emerge when mitochondrial haplotypes are in a cellular context without their coevolved nuclear-encoded mitochondrial (n-mt) proteins. Some case studies have shown that such disruptions in mitonuclear coevolution can contribute to reproductive isolation, but whether mitonuclear incompatibilities generate selection that impacts multiple n-mt loci and/or causes broad, genome-wide contributions to speciation is unclear. Here, we leverage a system with several hybridizing species pairs (Xiphophorus fishes) that have known mitonuclear incompatibilities of large effect. We divided nuclear-encoded genes into three classes based on level of interaction with mitochondrial gene products. We found only inconsistent statistical support for a difference between these classes in the degree of positive covariation in mitonuclear ancestry. We discuss evidence that these analyses are sensitive to the amount of non-synonymous divergence between parent species in interacting n-mt genes or the age of the hybridization event. Overall, our results imply that genome-wide scans focused on enrichment of broad functional gene classes may often be insufficient for detecting a history of mitonuclear coevolution, even when strong selection is acting on mitonuclear incompatibilities at multiple loci. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
MTALTCO1: a 259 amino-acid long mtDNA-encoded alternative protein that challenges conventional understandings of mitochondrial genomics.
Robitaille F, Campbell A, Ben Hadj A … +8 more , Cornet S, Nadeau-Lachance L, Niaison T, Choquette T, Nyffeler L, Roucou X, Angers A, Breton S
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923604 · Publisher ↗
Mitochondrial alternative open reading frames (ORFs) substantially broaden the functional scope traditionally attributed to mitochondrial DNA, encoding peptides and proteins that participate in diverse cellular processes...
Mitochondrial alternative open reading frames (ORFs) substantially broaden the functional scope traditionally attributed to mitochondrial DNA, encoding peptides and proteins that participate in diverse cellular processes. These newly identified ORFs are embedded within annotated sequences, both coding and non-coding, and reveal layers of overlapping genetic information. We report the discovery of MTALTCO1, a 259 amino-acid protein, the longest mitochondrial alternative protein identified to date, encoded by an ORF located within the human cytochrome oxidase 1 gene, in the +3 reading frame. We confirm the expression and mitochondrial origin of MTALTCO1 through multiple independent lines of evidence, including a custom-designed antibody, mass spectrometry-derived peptides, sequence analysis and inhibitors of mitochondrial expression. Despite encoding AGR codons as arginine, contrary to the prevailing view that these function invariably as stop codons in the vertebrate mitochondrial genetic code, MTALTCO1 shows strong evidence of mitochondrial translation, challenging established models of mitochondrial codon usage and gene expression. Co-immunoprecipitations and pulldown assays delineate MTALTCO1's interaction landscape across major cellular pathways. Finally, we present the first in-depth analysis of conservation for a mitochondrial alternative ORF overlapping a reference protein-coding gene and discuss the results in light of MTALTCO1's suggested role in protein scaffolding. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
The influence of size, longevity and environmental temperature on mitochondrial DNA evolution in fishes.
Le Cam S, Mortz M, Gagnier-Michel A … +2 more , Dufresne F, Blier PU
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923603 · Publisher ↗
The link between longevity and mitochondrial function has been documented; therefore, we suspect that the evolution of mitochondrial DNA (mtDNA) is linked to the evolution of longevity. We selected 128 fish species with...
The link between longevity and mitochondrial function has been documented; therefore, we suspect that the evolution of mitochondrial DNA (mtDNA) is linked to the evolution of longevity. We selected 128 fish species with a wide range of longevity and inhabiting habitats with differing temperatures and examined their association with dN/dS ratios of mtDNA genes. Our findings (i) rule out environmental temperature as a primary driver of longevity, (ii) confirm the negative relationship between synonymous substitution rate and longevity for four of the mitochondrial protein coding genes, (iii) reveal a correlation of the fish body length at maturity with the dN/dS ratio for ATP6, ND1 and ND4, and (iv) highlight for the first time to our knowledge, a link between high conservation of the three cytochrome c oxidase (COX) genes and adaptation to temperatures in fishes. By extending conclusions drawn from mtDNA to individual genes, our study opens new avenues for exploring the ageing process. Moreover, the specific link between the evolution of COX genes and habitat temperature confirms the importance of complex IV in temperature adaptation. Our findings also suggest a link between dN/dS in complex I genes and longevity, highlighting the need to examine the functional association between their encoded peptides and lifespan. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
Positive and relaxed selection on mitochondrial DNA in parasitic versus predatory mites.
Havird J, Wang E, Zwonitzer K … +3 more , Aitolo G, Xu X, Zhang B
Philos Trans R Soc Lond B Biol Sci · 2026 Apr · PMID 41923602 · Full text
Mitochondrial genomes (mtDNA) have distinct evolutionary trajectories owing to their inheritance, ploidy and underlying mutation rates, making them prone to accumulate slightly deleterious mutations. Positive selection o...
Mitochondrial genomes (mtDNA) have distinct evolutionary trajectories owing to their inheritance, ploidy and underlying mutation rates, making them prone to accumulate slightly deleterious mutations. Positive selection on mtDNA has been suggested to be important during adaptation to 'high-energy' lifestyles and environments. Disentangling positive versus relaxed selection in molecular mtDNA evolution studies is therefore important, although common metrics such as elevated dN/dS ratios (the ratio of non-synonymous to synonymous substitution rates) can be interpreted as signs of both relaxed purifying selection and positive selection. Here, we examined mtDNA evolution in mites (superorder Parasitiformes) to characterize selection during transitions from a parasitic to a free-living, predatory lifestyle. We predicted energetic demands on predatory mites would be associated with positive selection on mtDNA and that reduced effective population sizes in parasitic lineages would lead to relaxed selection. Using newly sequenced mite mitogenomes, we found a signature of accelerated mtDNA evolution in predatory lineages. Unexpectedly, this is likely due to relaxed, not positive selection on the mtDNA of predatory mites, which is supported by massive, ongoing gene rearrangements in the mtDNA of some predatory lineages (family Phytoseiidae). We discuss why 'high-energy' lifestyles are not always associated with adaptive mtDNA evolution. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.
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