Evolutionary Flexibility Research Articles

Transitions Into Freezing Environments Linked With Shifts in Phylogenetic Integration Between Vitaceae Leaf Traits.

Understanding how the intrinsic ability of populations and species to meet shifting selective demands shapes evolutionary patterns over both short and long timescales is a major question in biology. One major axis of evolutionary flexibility can be measured by phenotypic integration and modularity. The strength, scale, and structure of integration may constrain or catalyze evolution in the face of new selective pressures. We analyze a dataset of seven leaf measurements across Vitaceae to examine how correlations in trait divergence are linked to transitions between freezing and nonfreezing habitats. We assess this by applying a custom algorithm to compare the timing of habitat shifts to changes in the structure of evolutionary trait correlation at discrete points along a phylogeny. We also explore these patterns in relation to lineage diversification rates to understand how and whether patterns in the evolvability of complex multivariate phenotypes are linked to higher-level macroevolutionary dynamics. We found that shifts in the structure, but not the overall strength, of phylogenetic integration of leaves precipitate colonization of freezing climates. Lineages that underwent associated shifts in leaf trait integration and subsequent movement into freezing habitats also displayed lower turnover and higher net diversification, suggesting a link among shifting vectors of selection, internal constraint, and lineage persistence in the face of changing environments.

Light and temperature signals are integrated through a phyB-dependent gene regulatory network in rice.

Angiosperms are the most dominant land plant flora and have colonised most of the terrestrial habitats, thriving in different environmental conditions, among which light and temperature play a crucial role. In the eudicot Arabidopsis thaliana, light and temperature are integrated into a phytochrome B (phyB)-dependent signalling network that regulates development. However, whether this signal integration controls the development in other angiosperm lineages and if phyB is a conserved hub of this integratory network in angiosperms is unclear. We used a combination of phylogenetic, phenotypic, and transcriptomic analyses to understand the phyB-dependent light and temperature integratory network in the monocot Oryza sativa and infer its conservation in angiosperms. Here, we show that light and temperature co-regulate rice growth through a phyB-dependent regulatory network that shares conserved features between O. sativa and A. thaliana. Despite the conservation of the components of this regulatory network, the transcriptional regulation between the components has changed qualitatively since monocots and eudicots diverged (~192-145 MYA). The evolutionary flexibility of this integratory network might underlie the successful adaptation of plants to diverse ecological niches. Furthermore, our findings provide promising candidate genes whose activity and expression can be fine-tuned to improve plant growth and productivity in a warming planet.

Omicron-specific ultra-potent SARS-CoV-2 neutralizing antibodies targeting the N1/N2 loop of Spike N-terminal domain

A multitude of functional mutations continue to emerge on the N-terminal domain (NTD) of the spike protein in SARS-CoV-2 Omicron subvariants. Understanding the immunogenicity of Omicron NTD and the properties of antibodies elicited by it is crucial for comprehending the impact of NTD mutations on viral fitness and guiding vaccine design. In this study, we find that most of NTD-targeting antibodies isolated from individuals with BA.5/BF.7 breakthrough infection (BTI) are ancestral (wildtype or WT)-reactive and non-neutralizing. Surprisingly, we identified five ultra-potent neutralizing antibodies (NAbs) that can only bind to Omicron but not WT NTD. Structural analysis revealed that they bind to a unique epitope on the N1/N2 loop of NTD and interact with the receptor-binding domain (RBD) via the light chain. These Omicron-specific NAbs achieve neutralization through ACE2 competition and blockage of ACE2-mediated S1 shedding. However, BA.2.86 and BA.2.87.1, which carry insertions or deletions on the N1/N2 loop, can evade these antibodies. Together, we provided a detailed map of the NTD-targeting antibody repertoire in the post-Omicron era, demonstrating their vulnerability to NTD mutations enabled by its evolutionary flexibility, despite their potent neutralization. These results revealed the function of the indels in the NTD of BA.2.86/JN.1 sublineage in evading neutralizing antibodies and highlighted the importance of considering the immunogenicity of NTD in vaccine design.

Comparative analysis of two novel complete genomes of myxoma virus vaccine strains.

Myxoma virus (MYXV) is a double-stranded DNA-containing virus of the family Poxviridae, genus Leporipoxvirus. MYXV is an important model virus for evolutionary and immunological research and a promising oncolytic. In this study, we sequenced and analyzed two complete genomes of MYXV virus vaccine strains B-82 and Rabbivac-B, which are widely used for vaccine production in Russia. Here, we first show that MYXV vaccine strains B-82 and Rabbivac-B share a common origin with the American recombinant MYXV MAV vaccine strain. In addition, our data suggest that the MYXV B-82 and Rabbivac-B strains contain a number of genes at the 5' and 3' ends that are identical to the virulent MYXV Lausanne strain. Several unique genetic signatures were identified in the M013L, M017L, M023, and M121R genes, helping to achieve high genetic resolution between vaccine strains. Overall, these findings highlight the evolutionary flexibility of certain genes in the MYXV genome and provide insights into the molecular epidemiology of the virus and subsequent vaccine development.

Differential gene expression underpinning the production of distinct sperm morphs in the wax moth Galleria mellonella.

Male Lepidoptera produce two distinct sperm types; each ejaculate contains both eupyrene sperm, which can fertilize the egg, and apyrene sperm, which are not fertilization competent. These sperm have distinct morphologies, unique functions and different proteomes. Their production is highly regulated, however, very few genes with specific roles in the production of one or other morph have been described. We present the first comparative transcriptomics study of precursors of eupyrene and apyrene sperm to identify genes potentially implicated in regulating or enacting the distinct differentiation programmes. Differentially expressed genes included genes with potential roles in transcriptional regulation, cell cycle and sperm morphology. We identified gene duplications generating paralogues with functions restricted to one or other morph. However, phylogenetic analysis also revealed evolutionary flexibility in expression patterns of duplicated genes between different lepidopteran species. An improved understanding of lepidopteran reproduction will be vital in targeting prevalent pests in agriculture, and on the flip side, ensuring the fertility and thus survival of pollinator populations in response to environmental stress.

Sustainability in regulating biotechnology: A new form of knowledge in regulatory co‐production?

AbstractWe analyse the extent to which sustainable development influences the co‐production of regulations that target new technologies in the European Union (EU). We start by identifying the conventional forms of knowledge that serve as inputs into that co‐productive process, namely scientific, societal and legal knowledge. We show that sustainability‐related propositions have gained considerable traction in the regulation of genetic modification (GM) in the EU. Furthermore, the analysis reveals that sustainability cannot be reduced to scientific or societal knowledge. As far as the overlap between sustainability knowledge and legal knowledge is concerned, it is undeniable that sustainable development is deeply embedded into EU regulation; however, treating sustainable development solely as an element of the law does not capture the material influence that it exerts on society and technology, not to speak of its evolutionary flexibility. It follows that it would be best to treat sustainability as a separate input into the co‐creation process.

Evolutionary neurogenomics: Lengthy resolutions for complex brains

Genomic blueprints underlying unique neuronal organization are enigmatic. A new study reveals the recruitment of ancient, larger genes for synaptic machinery, providing evolutionary constraints and flexibility, with increasing gene sizes being found in animal lineages that led to cephalopods and vertebrates.

A cryptic syngameon within Betula shrubs revealed: Implications for conservation in changing subarctic environments.

Arctic and subarctic ecosystems are rapidly transforming due to global warming, emphasizing the need to understand the genetic diversity and adaptive strategies of northern plant species for effective conservation. This study focuses on Betula glandulosa, a native North American tundra shrub known as dwarf birch, which demonstrates an apparent capacity to adapt to changing climate conditions. To address the taxonomic challenges associated with shrub birches and logistical complexities of sampling in the northernmost areas where species' ranges overlap, we adopted a multicriteria approach. Incorporating molecular data, ploidy level assessment and leaf morphology, we aimed to distinguish B. glandulosa individuals from other shrub birch species sampled. Our results revealed three distinct species and their hybrids within the 537 collected samples, suggesting the existence of a shrub birch syngameon, a reproductive network of interconnected species. Additionally, we identified two discrete genetic clusters within the core species, B. glandulosa, that likely correspond to two different glacial lineages. A comparison between the nuclear and chloroplast SNP data emphasizes a long history of gene exchange between different birch species and genetic clusters. Furthermore, our results highlight the significance of incorporating interfertile congeneric species in conservation strategies and underscores the need for a holistic approach to conservation in the context of climate change, considering the complex dynamics of species interactions. While further research will be needed to describe this shrub birches syngameon and its constituents, this study is a first step in recognizing its existence and disseminating awareness among ecologists and conservation practitioners. This biological phenomenon, which offers evolutionary flexibility and resilience beyond what its constituent species can achieve individually, may have significant ecological implications.

Evolved Readers of 5‐Carboxylcytosine CpG Dyads Reveal a High Versatility of the Methyl‐CpG‐Binding Domain for Recognition of Noncanonical Epigenetic Marks

AbstractMammalian genomes are regulated by epigenetic cytosine (C) modifications in palindromic CpG dyads. Including canonical cytosine 5‐methylation (mC), a total of four different 5‐modifications can theoretically co‐exist in the two strands of a CpG, giving rise to a complex array of combinatorial marks with unique regulatory potentials. While tailored readers for individual marks could serve as versatile tools to study their functions, it has been unclear whether a natural protein scaffold would allow selective recognition of marks that vastly differ from canonical, symmetrically methylated CpGs. We conduct directed evolution experiments to generate readers of 5‐carboxylcytosine (caC) dyads based on the methyl‐CpG‐binding domain (MBD), the widely conserved natural reader of mC. Despite the stark steric and chemical differences to mC, we discover highly selective, low nanomolar binders of symmetric and asymmetric caC‐dyads. Together with mutational and modelling studies, our findings reveal a striking evolutionary flexibility of the MBD scaffold, allowing it to completely abandon its conserved mC recognition mode in favour of noncanonical dyad recognition, highlighting its potential for epigenetic reader design.

Evolved Readers of 5-Carboxylcytosine CpG Dyads Reveal a High Versatility of the Methyl-CpG-Binding Domain for Recognition of Noncanonical Epigenetic Marks.

Mammalian genomes are regulated by epigenetic cytosine (C) modifications in palindromic CpG dyads. Including canonical cytosine 5-methylation (mC), a total of four different 5-modifications can theoretically co-exist in the two strands of a CpG, giving rise to a complex array of combinatorial marks with unique regulatory potentials. While tailored readers for individual marks could serve as versatile tools to study their functions, it has been unclear whether a natural protein scaffold would allow selective recognition of marks that vastly differ from canonical, symmetrically methylated CpGs. We conduct directed evolution experiments to generate readers of 5-carboxylcytosine (caC) dyads based on the methyl-CpG-binding domain (MBD), the widely conserved natural reader of mC. Despite the stark steric and chemical differences to mC, we discover highly selective, low nanomolar binders of symmetric and asymmetric caC-dyads. Together with mutational and modelling studies, our findings reveal a striking evolutionary flexibility of the MBD scaffold, allowing it to completely abandon its conserved mC recognition mode in favour of noncanonical dyad recognition, highlighting its potential for epigenetic reader design.

Evolutionary flexibility and rigidity in the bacterial methylerythritol phosphate (MEP) pathway.

Terpenoids are a diverse class of compounds with wide-ranging uses including as industrial solvents, pharmaceuticals, and fragrances. Efforts to produce terpenoids sustainably by engineering microbes for fermentation are ongoing, but industrial production still largely relies on nonrenewable sources. The methylerythritol phosphate (MEP) pathway generates terpenoid precursor molecules and includes the enzyme Dxs and two iron-sulfur cluster enzymes: IspG and IspH. IspG and IspH are rate limiting-enzymes of the MEP pathway but are challenging for metabolic engineering because they require iron-sulfur cluster biogenesis and an ongoing supply of reducing equivalents to function. Therefore, identifying novel alternatives to IspG and IspH has been an on-going effort to aid in metabolic engineering of terpenoid biosynthesis. We report here an analysis of the evolutionary diversity of terpenoid biosynthesis strategies as a resource for exploration of alternative terpenoid biosynthesis pathways. Using comparative genomics, we surveyed a database of 4,400 diverse bacterial species and found that some may have evolved alternatives to the first enzyme in the pathway, Dxs making it evolutionarily flexible. In contrast, we found that IspG and IspH are evolutionarily rigid because we could not identify any species that appear to have enzymatic routes that circumvent these enzymes. The ever-growing repository of sequenced bacterial genomes has great potential to provide metabolic engineers with alternative metabolic pathway solutions. With the current state of knowledge, we found that enzymes IspG and IspH are evolutionarily indispensable which informs both metabolic engineering efforts and our understanding of the evolution of terpenoid biosynthesis pathways.

Dynamics of imprinted genes and their epigenetic mechanisms in castor bean seed with persistent endosperm.

Genomic imprinting refers to parent-of-origin-dependent gene expression and primarily occurs in the endosperm of flowering plants, but its functions and epigenetic mechanisms remain to be elucidated in eudicots. Castor bean, a eudicot with large and persistent endosperm, provides an excellent system for studying the imprinting. Here, we identified 131 imprinted genes in developing endosperms and endosperm at seed germination phase of castor bean, involving into the endosperm development, accumulation of storage compounds and specially seed germination. Our results showed that the transcriptional repression of maternal allele of DNA METHYLTRANSFERASE 1 (MET1) may be required for maternal genome demethylation in the endosperm. DNA methylation analysis showed that only a small fraction of imprinted genes was associated with allele-specific DNA methylation, and most of them were closely associated with constitutively unmethylated regions (UMRs), suggesting a limited role for DNA methylation in controlling genomic imprinting. Instead, histone modifications can be asymmetrically deposited in maternal and paternal genomes in a DNA methylation-independent manner to control expression of most imprinted genes. These results expanded our understanding of the occurrence and biological functions of imprinted genes and showed the evolutionary flexibility of the imprinting machinery and mechanisms in plants.

The divergence of mutation rates and spectra across the Tree of Life.

Owing to advances in genome sequencing, genome stability has become one of the most scrutinized cellular traits across the Tree of Life. Despite its centrality to all things biological, the mutation rate (per nucleotide site per generation) ranges over three orders of magnitude among species and several-fold within individual phylogenetic lineages. Within all major organismal groups, mutation rates scale negatively with the effective population size of a species and with the amount of functional DNA in the genome. This relationship is most parsimoniously explained by the drift-barrier hypothesis, which postulates that natural selection typically operates to reduce mutation rates until further improvement is thwarted by the power of random genetic drift. Despite this constraint, the molecular mechanisms underlying DNA replication fidelity and repair are free to wander, provided the performance of the entire system is maintained at the prevailing level. The evolutionary flexibility of the mutation rate bears on the resolution of several prior conundrums in phylogenetic and population-genetic analysis and raises challenges for future applications in these areas.

Comparing migratory connectivity across species: The importance of considering the pattern of sampling and the processes that lead to connectivity

Measuring the degree of migratory connectivity – how much and where different populations of species mix as they migrate over their annual cycle – is important because it informs the understanding of the evolution of migration, how populations will be affected by both habitat and climate change, and which areas to prioritize for conservation. But existing measures of connectivity may be difficult to compare because they measure different things and are confounded by sampling bias. Here we use tagging data from all available published landbird tracks up to July 2019 (224 populations, 86 species and 1524 individuals tracked in the three main global flyways) to identify robust measures to compare migratory connectivity across species. We consider two widely used descriptive measures: (1) degree of breeding population overlap on the non‐breeding grounds and (2) Mantel correlation, which tests the degree of spatial autocorrelation between the breeding and non‐breeding individuals; as well as one causative measure of the main process that leads to connectivity patterns: migratory spread of individuals from the same breeding population across the non‐breeding area. We investigated the sensitivity of these three measures to the distance between breeding locations of sampled populations (breeding distance) and their sample size. We also considered the confounding effects of migration distance because longer migrations decreased overlap and increased Mantel correlations and migratory spread. We found that the degree of overlap between breeding populations on the non‐breeding grounds decreased with increasing breeding distance and increased with increasing sample size. Mantel correlation coefficients also increased significantly with increasing breeding distance; sample size did not affect accuracy, but precision was greatly improved above a sample size of about 15 individuals. Migratory spread, however, was independent of breeding distance; sample size had only small effects on accuracy and precision, with no significant effects when more than four individuals per population were included. Furthermore, migratory spread was highly positively correlated with the maximum non‐breeding range. Overlap and Mantel correlations were highly confounded by the spatial pattern and amount of sampling, whereas migratory spread was relatively unconfounded, even by migratory distance. Although any descriptive migratory connectivity measure can help set priorities by determining current areas for conservation on the non‐breeding grounds, migratory spread, which leads to these patterns, needs fewer data, is comparable, and gives information on evolutionary flexibility and so ability to deal with changing habitat and climate.

What snakes and caecilians have in common? Molecular interaction units and the independent origins of similar morphotypes in Tetrapoda.

Developmental pathways encompass transcription factors and cis-regulatory elements that interact as transcription factor-regulatory element (TF-RE) units. Independent origins of similar phenotypes likely involve changes in different parts of these units, a hypothesis promisingly tested addressing the evolution of the rib-associated lumbar (RAL) morphotype that characterizes emblematic animals such as snakes and elephants. Previous investigation in these lineages identified a polymorphism in the Homology region 1 [H1] enhancer of the Myogenic factor-5 [Myf5], which interacts with HOX10 proteins to modulate rib development. Here we address the evolution of TF-RE units focusing on independent origins of RAL morphotypes. We compiled an extensive database for H1-Myf5 and HOX10 sequences with two goals: (i) evaluate if the enhancer polymorphism is present in amphibians exhibiting the RAL morphotype and (ii) test a hypothesis of enhanced evolutionary flexibility mediated by TF-RE units, according to which independent origins of the RAL morphotype might involve changes in either component of the interaction unit. We identified the H1-Myf5 polymorphism in lineages that diverged around 340 Ma, including Lissamphibia. Independent origins of the RAL morphotype in Tetrapoda involved sequence variation in either component of the TF-RE unit, confirming that different changes may similarly affect the phenotypic outcome of a given developmental pathway.

Morphological integration and evolutionary potential of the primate shoulder: Variation among taxa and implications for genetic covariances with the basicranium, pelvis, and arm

Within the primate order, the morphology of the shoulder girdle is immensely variable and has been shown to reflect the functional demands of the upper limb. The observed morphological variation among extant primate taxa consequently has been hypothesized to be driven by selection for different functional demands. Evolutionary analyses of the shoulder girdle often assess this anatomical region, and its traits, individually, therefore implicitly assuming independent evolution of the shoulder girdle. However, the primate shoulder girdle has developmental and functional covariances with the basicranium and pelvic girdle that have been shown to potentially influence its evolution. It is unknown whether these relationships are similar or even present across primate taxa, and how they may affect morphological variation among primates. This study evaluates the strength of covariance and evolutionary potential across four anatomical regions: shoulder girdle, basicranium, pelvis, and distal humerus. Measures of morphological integration and evolutionary potential (conditioned covariance and evolutionary flexibility) are assessed across eight anthropoid primate taxa. Results demonstrate a consistent pattern of morphological constraint within paired anatomical regions across primates. Differences in evolutionary flexibility are observed among primate genera, with humans having the highest evolutionary potential overall. This pattern does not follow functional differences, but rather a separation between monkeys and apes. Therefore, evolutionary hypotheses of primate shoulder girdle morphological variation that evaluate functional demands alone may not account for the effect of these relationships. Collectively, our findings suggest differences in genetic covariance among anatomical regions may have contributed to the observable morphological variation among taxa.

Community science reveals links between migration arrival timing advance, migration distance and wing shape.

Substantial global data show that many taxa are shifting their phenologies in response to climate change. For birds, migration arrival dates in breeding regions have been shifting earlier, and there is evidence that both evolutionary adaptation and behavioural flexibility influence these shifts. As more efficient flyers may be able to demonstrate more flexibility to respond to changing conditions during migratory flight, we hypothesize that differences among passerine species in flight efficiency, as reflected by morphology, may be associated with the magnitude of shifts in arrival date in response to climate warming. We applied a logistic model to 18 years of eBird data to estimate mean arrival date for 44 common passerines migrating to northeast North America. We then used linear mixed-effects models to estimate changes in mean arrival date and compared these changes to morphological proxies for flight efficiency and migratory distance using phylogenetic generalized least squares models. On average, passerine species shifted their arrival dates 0.120 days earlier each year, with 27 of the 44 species shifting to significantly earlier arrival times, and two shifting to significantly later ones. Of the 15 species with non-significant shifts, 13 trended toward earlier arrivals. Longer migration distances and higher wing aspect ratios were associated with greater shifts toward earlier arrivals. Migration distance and aspect ratio were also significantly correlated to each other. This suggests that changes in arrival date are affected by factors pertaining to migratory flight over long distances namely, flight efficiency and migration distance. These traits may be able predict the magnitude of arrival date shift, and by extension identify species that are most at risk to climate change due to inflexible arrival timing.

Genome Context Influences Evolutionary Flexibility of Nearly Identical Type III Effectors in Two Phytopathogenic Pseudomonads.

Integrative Conjugative Elements (ICEs) are replicons that can insert and excise from chromosomal locations in a site-specific manner, can conjugate across strains, and which often carry a variety of genes useful for bacterial growth and survival under specific conditions. Although ICEs have been identified and vetted within certain clades of the agricultural pathogen Pseudomonas syringae, the impact of ICE carriage and transfer across the entire P. syringae species complex remains underexplored. Here we identify and vet an ICE (PmaICE-DQ) from P. syringae pv. maculicola ES4326, a strain commonly used for laboratory virulence experiments, demonstrate that this element can excise and conjugate across strains, and highlight that this element contains loci encoding multiple type III effector proteins. Moreover, genome context suggests that another ICE (PmaICE-AOAB) is highly similar in comparison with and found immediately adjacent to PmaICE-DQ within the chromosome of strain ES4326, and also contains multiple type III effectors. Lastly, we present passage data from in planta experiments that suggests that genomic plasticity associated with ICEs may enable strains to more rapidly lose type III effectors that trigger R-gene mediated resistance in comparison to strains where nearly isogenic effectors are not present in active ICEs. Taken together, our study sheds light on a set of ICE elements from P. syringae pv. maculicola ES4326 and suggests how genomic context may lead to different evolutionary dynamics for shared virulence genes between strains.

Morphological integration and cranial modularity in six genera of echimyid rodents (Rodentia: Echimyidae)

Abstract Rodents of the family Echimyidae present a wide variety of life histories and ecomorphological adaptations. This study evaluated morphological integration patterns, modularity, and evolutionary flexibility in six Echimyid genera representing ecomorphological extremes within the family. The relationships between traits were evaluated by comparing estimated covariance and correlations matrices of populations. The presence of modules was investigated by comparing the patterns of integration between traits and using hypothetical matrices based on shared development/function and masticatory stress. The results point to a common covariance and correlation pattern among the six echimyid genera, suggesting a conserved pattern of covariation (associations among traits) throughout the evolution of this group. The overall magnitude of integration, however, varied greatly. We also found a high degree of modularity in all six echimyid genera. Finally, we observed a clear association between flexibility, i.e., the ability of a species to respond to the direction of selection, with the overall magnitude of integration and degree of modularization. The results of this study provide hypotheses concerning the underlying effects of the association among traits, which may have facilitated or constrained the evolution of morphological variation in the diverse family Echimyidae.

Evolutionary flexibility in routes to mat formation by Pseudomonas.

Many bacteria form mats at the air-liquid interface of static microcosms. These structures typically involve the secretion of exopolysaccharides, the production of which is often controlled by the secondary messenger c-di-GMP. Mechanisms of mat formation have been particularly well characterized in Pseudomonas fluorescens SBW25; stimuli or mutations that increase c-di-GMP production by diguanylate cyclases (WspR, AwsR, and MwsR) result in the secretion of cellulose and mat formation. Here, we characterize and compare mat formation in two close relatives of SBW25: Pseudomonas simiae PICF7 and P. fluorescens A506. We find that PICF7-the strain more closely related to SBW25-can form mats through mutations affecting the activity of the same three diguanylate cyclases as SBW25. However, instead of cellulose, these mutations activate production of the exopolysaccharide Pel. We also provide evidence for at least two further-as yet uncharacterized-routes to mat formation by PICF7. P. fluorescens A506, while retaining the same mutational routes to mat formation as SBW25 and PICF7, preferentially forms mats by a semi-heritable mechanism that culminates in Psl and Pga over-production. Our results demonstrate a high level of evolutionary flexibility in the molecular and structural routes to mat formation, even among close relatives.