Jonathan M Waters, Christopher P Burridge, David Craw, James S Albert
Recent genomic data highlight the key roles of geological processes in shaping the diversification and biogeography of freshwater lineages. Specifically, physical processes such as tectonic uplift, erosion, glaciation, lake formation, and sea-level fluctuation contribute extensively to the evolution of biotic diversity within and among drainages. River capture events can simultaneously isolate and merge lineages, with isolation potentially leading to speciation, and secondary contact enhancing alpha diversity within merged river reaches. The increased speciation rates of newly isolated lineages may be countered by their reduced population sizes and increased extinction risks. Knowledge of drainage history is essential for explaining freshwater biodiversity patterns, and also for understanding the drivers and temporal scales of biological evolution. Future interdisciplinary genomic and geological analyses are needed to understand and conserve freshwater biodiversity in a fast-changing world.
{"title":"Geological processes shaping freshwater biodiversity: a synthesis of global evidence.","authors":"Jonathan M Waters, Christopher P Burridge, David Craw, James S Albert","doi":"10.1002/brv.70135","DOIUrl":"https://doi.org/10.1002/brv.70135","url":null,"abstract":"<p><p>Recent genomic data highlight the key roles of geological processes in shaping the diversification and biogeography of freshwater lineages. Specifically, physical processes such as tectonic uplift, erosion, glaciation, lake formation, and sea-level fluctuation contribute extensively to the evolution of biotic diversity within and among drainages. River capture events can simultaneously isolate and merge lineages, with isolation potentially leading to speciation, and secondary contact enhancing alpha diversity within merged river reaches. The increased speciation rates of newly isolated lineages may be countered by their reduced population sizes and increased extinction risks. Knowledge of drainage history is essential for explaining freshwater biodiversity patterns, and also for understanding the drivers and temporal scales of biological evolution. Future interdisciplinary genomic and geological analyses are needed to understand and conserve freshwater biodiversity in a fast-changing world.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146111793","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Robert J Malka, Marcos Arranz, Ignacio Baselga-Carretero
Species from octopi to humans engage in play. This review examines how epigenetic mechanisms, such as DNA methylation, may regulate play behaviour across taxa. We frame play through historical definitions, categorizing it into object, locomotor, and social forms, and examine how each may be linked to epigenetic shifts, for example in brain-derived neurotrophic factor (BDNF) expression. We then explore the role of domestication in enhancing play via methylation of stress and sociality genes, comparing domesticated chickens, dogs, and foxes to their wild kin. We link the neurobiology of play, spanning the hypothalamic-pituitary-adrenal (HPA) axis and reward circuits, to epigenetic modulation. Assessing the evolutionary fitness advantages of play, we compare adaptive benefits against the surplus resource theory. Despite its presence in many taxa, there remains limited direct evidence for a role of epigenetic mechanisms in play, and we urge research into the developmental and adaptive roles of play across a wider range of species.
{"title":"Methylation and merriment: an exploration of epigenetic mechanisms underlying play behaviour.","authors":"Robert J Malka, Marcos Arranz, Ignacio Baselga-Carretero","doi":"10.1002/brv.70142","DOIUrl":"https://doi.org/10.1002/brv.70142","url":null,"abstract":"<p><p>Species from octopi to humans engage in play. This review examines how epigenetic mechanisms, such as DNA methylation, may regulate play behaviour across taxa. We frame play through historical definitions, categorizing it into object, locomotor, and social forms, and examine how each may be linked to epigenetic shifts, for example in brain-derived neurotrophic factor (BDNF) expression. We then explore the role of domestication in enhancing play via methylation of stress and sociality genes, comparing domesticated chickens, dogs, and foxes to their wild kin. We link the neurobiology of play, spanning the hypothalamic-pituitary-adrenal (HPA) axis and reward circuits, to epigenetic modulation. Assessing the evolutionary fitness advantages of play, we compare adaptive benefits against the surplus resource theory. Despite its presence in many taxa, there remains limited direct evidence for a role of epigenetic mechanisms in play, and we urge research into the developmental and adaptive roles of play across a wider range of species.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146111817","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Communication and sociality are intimately related, as many important social processes are mediated by communication between signal senders and receivers. Despite recent advances in social network analysis, animal communication networks remain difficult to characterize because the interactions that comprise the network structure depend on receiver sensory, perceptual, and cognitive processes. Collectively, these receiver psychological traits process social information and lead to decisions regarding whether and how to interact with signallers, generating variation in social interactions and the structure of communication networks. Here, we review the evidence that variation in receiver psychology affects both individuals' positions within the communication network and the structure of the communication network as a whole. These effects range from limits on signal active space imposed by receiver sensory acuity and sensitivity, to facilitation of social connections by learning and memory of signal characteristics. Although we identify numerous receiver psychological traits that likely affect connections between receivers and signallers, few studies have explicitly examined the role of receiver psychology on variation in communication network structure. We therefore review recent methodological advances that could facilitate such studies. We then show that the effects of receiver psychology on communication networks could have strong impacts on ecological and evolutionary processes. In particular, we discuss the reciprocal links between receiver psychology and social structure, and how these individual-group feedbacks are expected to generate coevolution between communication and sociality. Our review synthesizes diverse evidence that receiver psychology can affect communication interactions and provides a path forward for integrating sensory, perceptual, and cognitive mechanisms of signal processing with individual behavioural variation and ecological and evolutionary consequences of variation in animal social behaviour.
{"title":"Receiver psychology as a driver of communication network structure.","authors":"Michael S Reichert, Eleanor M Caves","doi":"10.1002/brv.70138","DOIUrl":"https://doi.org/10.1002/brv.70138","url":null,"abstract":"<p><p>Communication and sociality are intimately related, as many important social processes are mediated by communication between signal senders and receivers. Despite recent advances in social network analysis, animal communication networks remain difficult to characterize because the interactions that comprise the network structure depend on receiver sensory, perceptual, and cognitive processes. Collectively, these receiver psychological traits process social information and lead to decisions regarding whether and how to interact with signallers, generating variation in social interactions and the structure of communication networks. Here, we review the evidence that variation in receiver psychology affects both individuals' positions within the communication network and the structure of the communication network as a whole. These effects range from limits on signal active space imposed by receiver sensory acuity and sensitivity, to facilitation of social connections by learning and memory of signal characteristics. Although we identify numerous receiver psychological traits that likely affect connections between receivers and signallers, few studies have explicitly examined the role of receiver psychology on variation in communication network structure. We therefore review recent methodological advances that could facilitate such studies. We then show that the effects of receiver psychology on communication networks could have strong impacts on ecological and evolutionary processes. In particular, we discuss the reciprocal links between receiver psychology and social structure, and how these individual-group feedbacks are expected to generate coevolution between communication and sociality. Our review synthesizes diverse evidence that receiver psychology can affect communication interactions and provides a path forward for integrating sensory, perceptual, and cognitive mechanisms of signal processing with individual behavioural variation and ecological and evolutionary consequences of variation in animal social behaviour.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146111791","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alexander R Carey, Geoffrey J Cary, Teigan Cremona, Hugh F Davies, Brett P Murphy, Sam C Banks
Technological advances, including remote sensing, have led to a proliferation of metrics used in ecological studies to examine spatial patterns of fire regimes and their ecological effects. Researchers can use many different metrics to analyse spatial variation in both fire events and resulting fire regimes, including fire size, shape, intensity, frequency and seasonality. However, variation in metric selection, definition, and application can yield inconsistent findings and/or difficulty in the synthesis of findings from different studies. This review aims to (i) visualise trends in spatial terminology within the broader fire ecology literature, (ii) characterise the variability among metrics for describing spatial fire patterns, and (iii) evaluate the ecological relevance of metrics, identifying opportunities to enhance consistency. This review comprises three sections. First, we used topic modelling to determine topic trends in fire ecology over the last three decades (1991-2025). We found a shift from studies primarily focused on individual fire regime aspects to a more holistic approach incorporating multiple fire regime aspects, including spatial patterns. Second, we present findings from a qualitative review, revealing marked variation in metric selection within and among taxa, biomes, and the technique used to measure spatial metrics. We also identified ecological processes, such as dispersal capacity, that prompt researchers to use more specific metrics to analyse their study system more precisely, leading to less consistency among studies. Finally, we offer recommendations for enhancing metric consistency whilst maintaining the flexibility to adapt and develop those metrics most relevant and informative for a given objective. As technological advances allow for a more complete description of the spatial attributes of a fire regime, there is a potential trade-off between generality and precision, reducing comparability among studies. To ensure ecological relevance, it is crucial to consider the characteristics of data, landscape, and ecological contexts when selecting and applying metrics. Recent advances in landscape analysis techniques, such as through applying information theory, are leading to metrics that can be broadly applicable across study systems. Using the most generalised metrics possible, reporting standardised metrics of all fire regime components, aligning with landscape ecology where appropriate, and staying updated on emerging techniques will ensure the fire ecology field can move forward with a more coordinated approach.
{"title":"Spatial metrics in fire ecology: seeking consistency amidst complexity.","authors":"Alexander R Carey, Geoffrey J Cary, Teigan Cremona, Hugh F Davies, Brett P Murphy, Sam C Banks","doi":"10.1002/brv.70140","DOIUrl":"https://doi.org/10.1002/brv.70140","url":null,"abstract":"<p><p>Technological advances, including remote sensing, have led to a proliferation of metrics used in ecological studies to examine spatial patterns of fire regimes and their ecological effects. Researchers can use many different metrics to analyse spatial variation in both fire events and resulting fire regimes, including fire size, shape, intensity, frequency and seasonality. However, variation in metric selection, definition, and application can yield inconsistent findings and/or difficulty in the synthesis of findings from different studies. This review aims to (i) visualise trends in spatial terminology within the broader fire ecology literature, (ii) characterise the variability among metrics for describing spatial fire patterns, and (iii) evaluate the ecological relevance of metrics, identifying opportunities to enhance consistency. This review comprises three sections. First, we used topic modelling to determine topic trends in fire ecology over the last three decades (1991-2025). We found a shift from studies primarily focused on individual fire regime aspects to a more holistic approach incorporating multiple fire regime aspects, including spatial patterns. Second, we present findings from a qualitative review, revealing marked variation in metric selection within and among taxa, biomes, and the technique used to measure spatial metrics. We also identified ecological processes, such as dispersal capacity, that prompt researchers to use more specific metrics to analyse their study system more precisely, leading to less consistency among studies. Finally, we offer recommendations for enhancing metric consistency whilst maintaining the flexibility to adapt and develop those metrics most relevant and informative for a given objective. As technological advances allow for a more complete description of the spatial attributes of a fire regime, there is a potential trade-off between generality and precision, reducing comparability among studies. To ensure ecological relevance, it is crucial to consider the characteristics of data, landscape, and ecological contexts when selecting and applying metrics. Recent advances in landscape analysis techniques, such as through applying information theory, are leading to metrics that can be broadly applicable across study systems. Using the most generalised metrics possible, reporting standardised metrics of all fire regime components, aligning with landscape ecology where appropriate, and staying updated on emerging techniques will ensure the fire ecology field can move forward with a more coordinated approach.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146111822","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In recent years, complex technological capabilities have evolved, driven by the need to solve complex and integrative biological questions through global analyses. New equipment allows the scaling up and automation of processes which previously were carried out on a very limited scale. Concomitant with the availability of sophisticated technology developed to increase experimental processes in parallel, it is essential to have a versatile biological model that allows us to generate and handle large collections of genetic variants with the greatest possible capacity. This is a critical aspect in order to approach saturation levels in each search, to minimise false-positive and false-negative rates. In this sense, yeasts represent a prototypical eukaryotic model with a remarkable genome editing potential: it is possible to generate and phenotype several thousand genetically diverse strains on a high-throughput scale. Here we review, with a focus on the most recent years, the combination of the power of yeasts with the technical advances in multi-level processing capability. This has resulted in unprecedented global mappings of a multitude of biological processes with important implications that reshape our knowledge of fundamental biology, evolution and biotechnological/biomedical applications.
{"title":"The power of many: when genetics met yeasts and high-throughput.","authors":"Víctor A Tallada, Víctor Carranco","doi":"10.1002/brv.70141","DOIUrl":"https://doi.org/10.1002/brv.70141","url":null,"abstract":"<p><p>In recent years, complex technological capabilities have evolved, driven by the need to solve complex and integrative biological questions through global analyses. New equipment allows the scaling up and automation of processes which previously were carried out on a very limited scale. Concomitant with the availability of sophisticated technology developed to increase experimental processes in parallel, it is essential to have a versatile biological model that allows us to generate and handle large collections of genetic variants with the greatest possible capacity. This is a critical aspect in order to approach saturation levels in each search, to minimise false-positive and false-negative rates. In this sense, yeasts represent a prototypical eukaryotic model with a remarkable genome editing potential: it is possible to generate and phenotype several thousand genetically diverse strains on a high-throughput scale. Here we review, with a focus on the most recent years, the combination of the power of yeasts with the technical advances in multi-level processing capability. This has resulted in unprecedented global mappings of a multitude of biological processes with important implications that reshape our knowledge of fundamental biology, evolution and biotechnological/biomedical applications.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146091638","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Davis Laundon, Neil J Gostling, Ian G Reddin, Bram G Sengers, Pascale Chavatte-Palmer, Rohan M Lewis
Among the vertebrates, mammals are notable for the dominance of live birth and placental nutrition. The structural diversity of the mammalian placenta is remarkable, despite sharing a single common ancestor and conserved physiological functions. Historically, investigations into the evolution of the mammalian placenta have been grounded in 'the efficiency paradigm', i.e. the assumption that certain placental configurations permit easier nutrient exchange, but this paradigm has struggled to explain the diversity of mammalian placentation strategies. Here, we propose a new paradigm to understand mammalian placental evolution. Using multidimensional plotting of recorded placental structures, quantitative metrics for mammalian maternal investment, and illustrative computational modelling of physiological processes, we argue that the ancestral mammalian placenta is not a streamlined 'highly efficient' design, but rather a product of low maternal investment, with fitness costs that manifest as gestational demand increases. Expansion of small mammals into larger-bodied, longer-lived niches induces a 'placental crisis' characterised by maternal under-investment and chronic gestational dysfunction, triggering an arms race through the interaction of disruptive selection and materno-fetal conflict. We propose the acute severity of the placental crisis is the foundation of placental evolution. We go on to argue that some primates are currently in a state of placental crisis and that maternal under-investment and inappropriate placentation are the evolutionary foundations of human gestational dysfunctions such as pre-eclampsia. We conclude that the ancestral mammalian placenta was not an efficiently optimised design that allowed placentation to dominate the clade, but rather an idiosyncrasy of mammal-specific biology, which likely hindered mammalian expansion into larger-bodied niches.
{"title":"Placental crises: disruptive selection and maternal under-investment as the foundations of mammalian placental evolution and dysfunction.","authors":"Davis Laundon, Neil J Gostling, Ian G Reddin, Bram G Sengers, Pascale Chavatte-Palmer, Rohan M Lewis","doi":"10.1002/brv.70139","DOIUrl":"https://doi.org/10.1002/brv.70139","url":null,"abstract":"<p><p>Among the vertebrates, mammals are notable for the dominance of live birth and placental nutrition. The structural diversity of the mammalian placenta is remarkable, despite sharing a single common ancestor and conserved physiological functions. Historically, investigations into the evolution of the mammalian placenta have been grounded in 'the efficiency paradigm', i.e. the assumption that certain placental configurations permit easier nutrient exchange, but this paradigm has struggled to explain the diversity of mammalian placentation strategies. Here, we propose a new paradigm to understand mammalian placental evolution. Using multidimensional plotting of recorded placental structures, quantitative metrics for mammalian maternal investment, and illustrative computational modelling of physiological processes, we argue that the ancestral mammalian placenta is not a streamlined 'highly efficient' design, but rather a product of low maternal investment, with fitness costs that manifest as gestational demand increases. Expansion of small mammals into larger-bodied, longer-lived niches induces a 'placental crisis' characterised by maternal under-investment and chronic gestational dysfunction, triggering an arms race through the interaction of disruptive selection and materno-fetal conflict. We propose the acute severity of the placental crisis is the foundation of placental evolution. We go on to argue that some primates are currently in a state of placental crisis and that maternal under-investment and inappropriate placentation are the evolutionary foundations of human gestational dysfunctions such as pre-eclampsia. We conclude that the ancestral mammalian placenta was not an efficiently optimised design that allowed placentation to dominate the clade, but rather an idiosyncrasy of mammal-specific biology, which likely hindered mammalian expansion into larger-bodied niches.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146091588","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gain curves have been a staple of sex allocation theory for decades. They represent patterns in which fitness is obtained from resource investments in reproductive functions. The monotonic forms that have been used for gain curves can represent fitness accrual by individuals, but only on the assumption that sufficient mates are always available to allow the stipulated monotonic pattern of reproductive success to occur. However, sexual populations do not have external banks of mating opportunities that lie outside the dynamics of the population (such opportunities would, by definition, be part of the population). Thus, the reproductive behaviour of whole populations cannot be simple scaled-up versions of individual gain curves. As sex allocation evolves within a breeding population, frequency-dependent selection creates a shifting advantage for the rarer sex. Individual gain curves cannot then remain stable possibilities at the population level. Evolutionary models based on fixed gain curves can predict evolutionary outcomes with unequal total fitness for male and for female function, an outcome that the biology of syngamy does not allow. Such biologically impossible outcomes are easily demonstrated. Gain curves have also been widely used as a framework for interpretation of interspecific empirical patterns, such as low male allocation in monogamously mating hermaphroditic animals or self-pollinating plants, and higher male allocation in wind-pollinated than in animal-pollinated plants. However, if gain curves incorrectly characterize whole populations or species, interspecific differences in gain curves cannot explain these patterns. Even if they superficially appear to predict the empirical pattern, other processes must be operating. The selective effects of local mating competition and sex-specific dispersal patterns have long been known. They are likely replacements for gain curves as explanations of many broad interspecific patterns, but the predominance of gain-curve explanations has distracted attention from these alternatives. A revision of our understanding of gain curves seems needed.
{"title":"The nature of gain curves.","authors":"Martin Burd","doi":"10.1002/brv.70136","DOIUrl":"https://doi.org/10.1002/brv.70136","url":null,"abstract":"<p><p>Gain curves have been a staple of sex allocation theory for decades. They represent patterns in which fitness is obtained from resource investments in reproductive functions. The monotonic forms that have been used for gain curves can represent fitness accrual by individuals, but only on the assumption that sufficient mates are always available to allow the stipulated monotonic pattern of reproductive success to occur. However, sexual populations do not have external banks of mating opportunities that lie outside the dynamics of the population (such opportunities would, by definition, be part of the population). Thus, the reproductive behaviour of whole populations cannot be simple scaled-up versions of individual gain curves. As sex allocation evolves within a breeding population, frequency-dependent selection creates a shifting advantage for the rarer sex. Individual gain curves cannot then remain stable possibilities at the population level. Evolutionary models based on fixed gain curves can predict evolutionary outcomes with unequal total fitness for male and for female function, an outcome that the biology of syngamy does not allow. Such biologically impossible outcomes are easily demonstrated. Gain curves have also been widely used as a framework for interpretation of interspecific empirical patterns, such as low male allocation in monogamously mating hermaphroditic animals or self-pollinating plants, and higher male allocation in wind-pollinated than in animal-pollinated plants. However, if gain curves incorrectly characterize whole populations or species, interspecific differences in gain curves cannot explain these patterns. Even if they superficially appear to predict the empirical pattern, other processes must be operating. The selective effects of local mating competition and sex-specific dispersal patterns have long been known. They are likely replacements for gain curves as explanations of many broad interspecific patterns, but the predominance of gain-curve explanations has distracted attention from these alternatives. A revision of our understanding of gain curves seems needed.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146083646","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
<p><p>The seed is an essential stage in the life history of gymnospermous and angiospermous plants, facilitating both their survival and dispersal. We reappraise knowledge of the evolutionary history of the gymnospermous seed, from its origin in the late Devonian through to the well-known end-Permian extinctions - an interval encompassing the origins of most major lineages of seed-bearing plants. The framework for our broader discussions is a novel cladistic analysis of anatomically preserved Palaeozoic seeds, analysing 79 seed-species for 89 morphological characters in a matrix containing only 24% missing values. The resulting consensus tree is weakly but fully resolved and compatible with traditional division into three informal seed groups: paraphyletic lagenocarps, paraphyletic trigonocarps and monophyletic cardiocarps. Three seed-genera - Rhychosperma, Albertlongia and Muricosperma - are revealed as potential 'missing links' between groups, and modest re-circumscription of seed-genera is required. Although the value of single-organ phylogenies remains controversial, the present seed-tree topology receives general support from the dated sequence of first appearances of seed-species in the fossil record, and from the topologies of morphological cladistic studies that combined conceptually reconstructed fossil plants with primitive extant lineages, notably ginkgos and cycads. Branch lengths in the tree and phenetic distances in ordinations of the matrix indicate similar overall rates of character change through the Palaeozoic, rather than a fractal pattern reflecting progressively increasing constraint, although early changes in architectural and pollination-related characters gradually give way to greater experimentation with the internal layering and external topography of the testa. Our process-based evolutionary inferences are informed by extant gymnosperms, particularly Cycas and Ginkgo. The origin of the true seed is attributed primarily to (1) the complex biochemical signalling needed to allow the sperm to reach the archegonia through the megasporangium wall and (2) the localised apoptosis of the megasporangium hypothesised to have simultaneously allowed hollowing out of the nucellar apex to form a sophisticated pollen-receiving apparatus (the pollen chamber) and secretion of a pollination drop to capture air-borne (pre)pollen. Subsequent potential key innovations include transfer of function of both pollination-drop channelling and pollen chamber sealing from the nucellar salpinx to the integumentary micropyle, and introduction of a haustorial pollen tube to direct spermatozoa towards the archegonia. Assuming that the seed-plant megasporangium terminates an axis, synorganisation has played a key role in seed evolution, leaf-like lateral organs being repeatedly pulled towards the apex and incorporated into the terminal structure. Lateral webbing of integumentary lobes eventually almost fully enclosed the nucellus, while a similar synorga
{"title":"Early evolutionary history of the seed.","authors":"Richard M Bateman, Alan R T Spencer, Jason Hilton","doi":"10.1002/brv.70134","DOIUrl":"https://doi.org/10.1002/brv.70134","url":null,"abstract":"<p><p>The seed is an essential stage in the life history of gymnospermous and angiospermous plants, facilitating both their survival and dispersal. We reappraise knowledge of the evolutionary history of the gymnospermous seed, from its origin in the late Devonian through to the well-known end-Permian extinctions - an interval encompassing the origins of most major lineages of seed-bearing plants. The framework for our broader discussions is a novel cladistic analysis of anatomically preserved Palaeozoic seeds, analysing 79 seed-species for 89 morphological characters in a matrix containing only 24% missing values. The resulting consensus tree is weakly but fully resolved and compatible with traditional division into three informal seed groups: paraphyletic lagenocarps, paraphyletic trigonocarps and monophyletic cardiocarps. Three seed-genera - Rhychosperma, Albertlongia and Muricosperma - are revealed as potential 'missing links' between groups, and modest re-circumscription of seed-genera is required. Although the value of single-organ phylogenies remains controversial, the present seed-tree topology receives general support from the dated sequence of first appearances of seed-species in the fossil record, and from the topologies of morphological cladistic studies that combined conceptually reconstructed fossil plants with primitive extant lineages, notably ginkgos and cycads. Branch lengths in the tree and phenetic distances in ordinations of the matrix indicate similar overall rates of character change through the Palaeozoic, rather than a fractal pattern reflecting progressively increasing constraint, although early changes in architectural and pollination-related characters gradually give way to greater experimentation with the internal layering and external topography of the testa. Our process-based evolutionary inferences are informed by extant gymnosperms, particularly Cycas and Ginkgo. The origin of the true seed is attributed primarily to (1) the complex biochemical signalling needed to allow the sperm to reach the archegonia through the megasporangium wall and (2) the localised apoptosis of the megasporangium hypothesised to have simultaneously allowed hollowing out of the nucellar apex to form a sophisticated pollen-receiving apparatus (the pollen chamber) and secretion of a pollination drop to capture air-borne (pre)pollen. Subsequent potential key innovations include transfer of function of both pollination-drop channelling and pollen chamber sealing from the nucellar salpinx to the integumentary micropyle, and introduction of a haustorial pollen tube to direct spermatozoa towards the archegonia. Assuming that the seed-plant megasporangium terminates an axis, synorganisation has played a key role in seed evolution, leaf-like lateral organs being repeatedly pulled towards the apex and incorporated into the terminal structure. Lateral webbing of integumentary lobes eventually almost fully enclosed the nucellus, while a similar synorga","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146049601","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sébastien Mirolo, Alice Ledent, Juana M González-Mancebo, Rosalina Gabriel, Manuela Sim-Sim, Flavien Collart, Jairo Patiño, Alain Vanderpoorten
Endemism, a hallmark of island biodiversity, reaches its lowest levels among bryophytes compared with other land plants. Whether this pattern reflects low diversification rates, and why, or whether it is a result of loss of endemicity due to extinctions or subsequent continental (back-)colonization, is examined here through a review of available evidence in the Macaronesian flora. Significant genetic differentiation (GST, based on allele frequencies) was consistently found between Macaronesian and continental populations, ruling out the hypothesis that intense migrations necessarily hamper differentiation. A significant phylogeographical signal in the data (NST > GST; where NST is a GST analog incorporating phylogenetic relationships among alleles), involving higher mutation rates than dispersal rates and evidencing incipient speciation, was further found in more than 1/3 of the species investigated. The significantly higher average NST between extra-European regions and Macaronesia compared to Europe and Macaronesia suggests, however, that incipient speciation is more likely to occur between distant (Macaronesian versus extra-European) than closer (Macaronesian versus European) populations. In line with this, ancestral area estimations in Macaronesian endemic bryophyte species revealed that at least 50% of them have an extra-European origin, in contrast with the almost exclusively (>90%) European/Mediterranean origin of Macaronesian endemic spermatophytes. Allopatric speciation via long-distance dispersal and subsequent divergence of a single endemic species prevails in island bryophytes, wherein sympatric radiations virtually never occur. Such a speciation mode does not trigger high rates of endemism, in contrast to radiations in Macaronesian spermatophytes, which contribute to 56% of the total number of endemics. Several mechanisms may explain the failure of island bryophytes to diversify in situ, including the fact that oceanic islands are too small or insufficiently isolated from each other or from continents to promote sympatric speciation, the lack of key innovations, and phylogenetic niche conservatism for stable habitats not prone to trigger radiations. In comparison with spermatophytes, continental (back-)colonization further largely prevails in bryophytes and, unlike in many instances in angiosperms, is not followed by in situ speciation on the mainland. The consequent loss of the endemic status of species that did speciate on islands but subsequently enlarged their range further accounts for the low rates of endemism among island bryophyte floras and invalidates the use of endemism rates as a proxy of speciation rates in this group.
{"title":"Why are so few island bryophytes endemic?","authors":"Sébastien Mirolo, Alice Ledent, Juana M González-Mancebo, Rosalina Gabriel, Manuela Sim-Sim, Flavien Collart, Jairo Patiño, Alain Vanderpoorten","doi":"10.1002/brv.70127","DOIUrl":"https://doi.org/10.1002/brv.70127","url":null,"abstract":"<p><p>Endemism, a hallmark of island biodiversity, reaches its lowest levels among bryophytes compared with other land plants. Whether this pattern reflects low diversification rates, and why, or whether it is a result of loss of endemicity due to extinctions or subsequent continental (back-)colonization, is examined here through a review of available evidence in the Macaronesian flora. Significant genetic differentiation (G<sub>ST</sub>, based on allele frequencies) was consistently found between Macaronesian and continental populations, ruling out the hypothesis that intense migrations necessarily hamper differentiation. A significant phylogeographical signal in the data (N<sub>ST</sub> > G<sub>ST</sub>; where N<sub>ST</sub> is a G<sub>ST</sub> analog incorporating phylogenetic relationships among alleles), involving higher mutation rates than dispersal rates and evidencing incipient speciation, was further found in more than 1/3 of the species investigated. The significantly higher average N<sub>ST</sub> between extra-European regions and Macaronesia compared to Europe and Macaronesia suggests, however, that incipient speciation is more likely to occur between distant (Macaronesian versus extra-European) than closer (Macaronesian versus European) populations. In line with this, ancestral area estimations in Macaronesian endemic bryophyte species revealed that at least 50% of them have an extra-European origin, in contrast with the almost exclusively (>90%) European/Mediterranean origin of Macaronesian endemic spermatophytes. Allopatric speciation via long-distance dispersal and subsequent divergence of a single endemic species prevails in island bryophytes, wherein sympatric radiations virtually never occur. Such a speciation mode does not trigger high rates of endemism, in contrast to radiations in Macaronesian spermatophytes, which contribute to 56% of the total number of endemics. Several mechanisms may explain the failure of island bryophytes to diversify in situ, including the fact that oceanic islands are too small or insufficiently isolated from each other or from continents to promote sympatric speciation, the lack of key innovations, and phylogenetic niche conservatism for stable habitats not prone to trigger radiations. In comparison with spermatophytes, continental (back-)colonization further largely prevails in bryophytes and, unlike in many instances in angiosperms, is not followed by in situ speciation on the mainland. The consequent loss of the endemic status of species that did speciate on islands but subsequently enlarged their range further accounts for the low rates of endemism among island bryophyte floras and invalidates the use of endemism rates as a proxy of speciation rates in this group.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146045764","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Helena Norman, Daphne Cortese, Amelia Munson, Jan Lindström, Shaun S Killen
Basal and standard metabolic rate (BMR and SMR) are cornerstones of physiological ecology and are assumed to be relatively fixed intrinsic properties of organisms that represent the minimum energy required to sustain life. However, this assumption is conceptually flawed. Many core maintenance processes underlying SMR are temporally partitioned across sleep and wakefulness and are not continuously active. We argue that instead of representing a singular metabolic state, SMR is better defined as a shifting metabolic mosaic where maintenance functions are distributed unevenly across different sleep-wake states, including metabolically and functionally distinct phases such as non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. SMR measured during wakefulness will mainly represent ion regulation, thermoregulation, sensory processing, and substrate cycling. Meanwhile, SMR measured during sleep primarily includes processes upregulated during sleep, including protein synthesis, cellular repair, immunity, and synaptic plasticity. Our models demonstrate that SMR values measured exclusively during wake or sleep consistently over- or underestimate daily maintenance costs depending on the time spent in specific sleep states and when SMR was measured. In addition, treatment or environmental effects on the costs of specific processes may be entirely missed if metabolic measures occur during an inappropriate sleep-wake state. The temporal partitioning of maintenance processes suggests that traditional and current approaches to SMR measurement may confound true metabolic variation with individual and species-specific differences in sleep architecture, with implications for the estimation of energy budgets, trait heritability, environmental effects on metabolic rate, and metabolic scaling relationships. We propose redefining organismal maintenance costs as a time-integrated profile of metabolic demands, but also suggest that state-specific SMR measurements are appropriate if the sleep-wake measurement period aligns with that of the behavioural, physiological, or ecological context of interest. Moving beyond the fiction of a constant maintenance baseline would provide more refined insights into the bioenergetic foundations of ecological performance and evolutionary constraints.
{"title":"The myth of the metabolic baseline: sleep-wake cycles undermine a foundational assumption in organismal biology.","authors":"Helena Norman, Daphne Cortese, Amelia Munson, Jan Lindström, Shaun S Killen","doi":"10.1002/brv.70133","DOIUrl":"https://doi.org/10.1002/brv.70133","url":null,"abstract":"<p><p>Basal and standard metabolic rate (BMR and SMR) are cornerstones of physiological ecology and are assumed to be relatively fixed intrinsic properties of organisms that represent the minimum energy required to sustain life. However, this assumption is conceptually flawed. Many core maintenance processes underlying SMR are temporally partitioned across sleep and wakefulness and are not continuously active. We argue that instead of representing a singular metabolic state, SMR is better defined as a shifting metabolic mosaic where maintenance functions are distributed unevenly across different sleep-wake states, including metabolically and functionally distinct phases such as non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. SMR measured during wakefulness will mainly represent ion regulation, thermoregulation, sensory processing, and substrate cycling. Meanwhile, SMR measured during sleep primarily includes processes upregulated during sleep, including protein synthesis, cellular repair, immunity, and synaptic plasticity. Our models demonstrate that SMR values measured exclusively during wake or sleep consistently over- or underestimate daily maintenance costs depending on the time spent in specific sleep states and when SMR was measured. In addition, treatment or environmental effects on the costs of specific processes may be entirely missed if metabolic measures occur during an inappropriate sleep-wake state. The temporal partitioning of maintenance processes suggests that traditional and current approaches to SMR measurement may confound true metabolic variation with individual and species-specific differences in sleep architecture, with implications for the estimation of energy budgets, trait heritability, environmental effects on metabolic rate, and metabolic scaling relationships. We propose redefining organismal maintenance costs as a time-integrated profile of metabolic demands, but also suggest that state-specific SMR measurements are appropriate if the sleep-wake measurement period aligns with that of the behavioural, physiological, or ecological context of interest. Moving beyond the fiction of a constant maintenance baseline would provide more refined insights into the bioenergetic foundations of ecological performance and evolutionary constraints.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":" ","pages":""},"PeriodicalIF":11.7,"publicationDate":"2026-01-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146027914","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}