[Evolutionary novelties in the display of pigeon breeds (Columba livia var. domestica) as a result of selective breeding by man].
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The irreversibility of complex trait loss has long been a tenet of evolutionary biology. However, this idea is increasingly at odds with the numerous documented exceptions across the Tree of Life. We synthesise this growing body of evidence across a diverse array of taxa and traits, exploring the evolutionary conditions that enable evolutionary reversal. By integrating macroevolutionary, genetic, and developmental information, we argue that trait reversal is commonly fostered by some form of persistence in the generative developmental pathway of the lost trait. We identify three overarching modes of trait reversal and support them with multiple case studies: by pleiotropy (the involvement of the same generative components in other traits and/or functions), by plasticity (environment-dependent expression of the trait) and by hemiplasy (persistence in another lineage, followed by reticulate evolution). We also examine important affinities between trait reversal and evolutionary novelties, undermining a neat distinction between what is old and what is new in evolution. This survey may provide a useful framework for future explorations of the developmental mechanisms underlying these still overlooked macroevolutionary dynamics.
Mutations are the source of evolutionary novelty but also the cause of genetic diseases and cancer. Mutation rates are known to be heterogeneous along the genome, however the extent to which local mutation rates vary among individuals in a population and are genetically determined is unknown. To test this, we analyzed the chromosomal distribution of somatic mutations in cell lines from 1,662 individuals, controlling for the confounding effects of DNA replication timing on local mutation rates and of trans-acting modulators on global mutation rates. We describe substantial interindividual variation in mutation rates across the human genome. By comparing mutation-rate variation to individuals' genotypes, we identified 35 instances in which polymorphic alleles in the population associate with somatic mutation rates in their vicinity. We call these mutation quantitative trait loci (mutQTLs). mutQTLs associated with somatic mutations in lymphoblastoid cell lines and in chronic lymphocytic leukemia, and with germline genetic variants. Two of the four mutQTLs inferred to be associated with germline mutation-rate variation were located within large clusters of zinc-finger genes and transposable elements, where they functioned as cis-mutators conferring an increased rate of mutation in their vicinity. mutQTLs provide a portal into the evolution of mutation rate heterogeneity across the genome and across individuals.
Hybridization is a widespread evolutionary process and a key source of evolutionary novelty. Despite intensive study, the extent to which hybridization is deterministic and repeatable, particularly in recurrent contact events involving the same species under varying ecological conditions, remains unclear. Here, we investigated three replicated contact zones between Scots pine (Pinus sylvestris) and dwarf mountain pine (Pinus mugo) in Central Europe: two occurring in peatland habitats and one in a contrasting sandstone outcrop. Using genome-wide SNP genotyping of over 1300 individuals, we analysed genomic structure, diversity, and ancestry patterns across these zones. All sites revealed pervasive hybridization, dominated by later-generation hybrids and a notable scarcity of pure P. mugo. Across environments, hybrid populations exhibited strikingly consistent genomic compositions, with asymmetric introgression strongly biased toward P. mugo ancestry, suggesting that hybrid genome structure may follow predictable patterns under similar ecological conditions and could be shaped by cytonuclear incompatibilities. Nonetheless, we also detected site-specific differences in hybrid diversity and phenotype, highlighting the influence of local environmental selection on shared hybrid genomic backgrounds. We provide genomic evidence that Pinus uliginosa, a morphologically distinct peat bog pine traditionally regarded as a relict and endangered species is instead a partially stabilised hybrid lineage. Its genome reflects incomplete hybridization and ecological filtering, yet it lacks sufficient genetic divergence to be recognised as a distinct species. Together, these results provide evidence for the repeatability of hybridization processes, which result in the formation of phenotypes reflecting a species continuum subjected to strong environmental pressures. The findings support the simplification of taxonomic nomenclature within the Pinus mugo complex, informing adaptive conservation strategies and the genetic management of hybrid lineages.
Evolutionary innovation is a catalyst for the colonization of new environments and the adaptive radiations of major groups. Novel traits typically evolve through the modification of preexisting characters, but the genetic paths underlying their origin have been challenging to trace, and the general requirements for and relative order of different kinds of gene mutations have been difficult to assess. Here, we trace the genomic origins of four procoagulant venom toxins (factor X, factor V, group I phospholipase A2, and Kunitz-type toxins) that collectively underlie a novel, especially potent blood-clotting venom type in the recently evolved Australian brown snake and taipan clade. We find evidence for a previously unknown fifth toxin, coagulation factor VII, and show that the toxins evolved through two distinct genetic paths. The factor X and factor V toxins evolved through the sequential de novo co-option of ancestral clotting factor proteins that entailed their heterotopic expression in the venom gland, the fixation of segmental duplications containing each locus, and subsequent gain-of-function mutations that rendered factor X and factor V constitutively active. In contrast, the phospholipase A2 and Kunitz-type toxins evolved by modifying the functions of neurotoxins that were part of the venom arsenal. Our findings support models in which innovative mutations in single-copy genes precede gene duplication in the evolution of novel proteins and offer a rare view into the genesis of a complex trait that has played a central role in a major adaptive radiation.
Evolutionary innovation is a key driver of the colonization of new environments and the adaptive radiations of major groups. Novel traits typically evolve through the modification of pre-existing characters but the genetic paths underlying their origin have been challenging to trace, and the general requirements for and relative order of different kinds of gene mutations have been difficult to assess. Here, we trace the genomic origins of four procoagulant venom toxins (factor X, factor V, group I phospholipase A2, and Kunitz-type toxins) that collectively underlie a novel, especially potent blood-clotting venom type in the recently evolved Australian brown snake and taipan clade. We discover evidence for a previously unknown fifth toxin, coagulation factor VII, and show that the toxins evolved through two distinct genetic paths. The factor X and factor V toxins evolved through the sequential de novo co-option of ancestral clotting factor proteins that entailed their heterotopic expression in the venom gland, the fixation of segmental duplications containing each locus, and subsequent gain-of-function mutations that rendered factor X and factor V constitutively active. In contrast, the phospholipase A2 and Kunitz-type toxins evolved by modifying the functions of neurotoxins that were part of the venom arsenal. Our findings support models in which innovative mutations in single-copy genes precede gene duplication in the evolution of novel proteins and offer a rare view into the genesis of a complex trait that has played a central role in a major adaptive radiation.
Current models for evolvability and complexity generally focus on mutational and regulatory processes in the host genome alone, limiting their ability to explain the origin, inheritance, and dynamics of many phenotypes. We describe a framework treating multigenome interactions in the holobiont as a central process that impacts the genotype-phenotype map, expanding the dimensionality of mechanisms producing heritable variation, generating novel traits, and exploring adaptive trajectories. These mechanisms can promote both complex phenotypic innovation and evolutionary systems drift. Many evolutionary pathways and novelties cannot be fully understood from host data alone but require consideration of hologenomic targets of selection. We outline hypotheses and methods to quantify and evaluate their impacts as a fundamental macroevolutionary process.
Wallin (1927) first published the notion that the fusion of bacteria with host cells was the principal source of genetic novelty for speciation. He suggested that mitochondria are transitional elements in this process. While the significance that he attributed to symbiosis now seem excessive, he was one of the first authors to be aware of the evolutionary potential of symbiotic events and his view of mitochondria may not seem strange to many cell biologist today. The most significant evolutionary development which has been attributed to intracellular symbiosis is the origin of eukaryotic cellular organization. The current status of the 'serial endosymbiosis hypothesis' is briefly review. The case for the symbiotic origin of the chloroplast, based principally on 16 S RNA oligonucleotide cataloguing, is very strong. Mitochondrial origins are more obscure but also appear to be symbiotic due to recent 18 S cataloguing from wheat embryos. The probablility of the multiple origin of some eukaryotic organelles is also examined, the processes in question being the acquisition of distinct stocks of chloroplasts from disparate photosynthetic prokaryotes and the secondary donation of organelles from degenerate eukaryotic endosymbionts to their hosts, with specific reference to the dinoflagellates Peridinium balticum, Kryptoperidinium foliaceum and the ciliate Mesodinium rubrum. It is concluded that the evolutionary potential of intracellular symbiosis ('cytobiosis': a term introduced in this paper) is great, with the best established influence being on the origin of eukaryotic chloroplasts. Together with the potential effects of viral vectors, symbiosis serves as a supplementary speciation mechanism capable of producing directed evolutionary changes. It is likely that these processes will explain some of the apparent anomalies in evolutionary rates and direction which are not readily explicable by the conventional synthetic theory of evolution.
How genomic changes translate into organismal novelties is often confounded by the multi-layered nature of genome architecture and the long evolutionary timescales over which molecular changes accumulate. Coleoid cephalopods (squid, cuttlefish, and octopus) provide a unique system to study these processes due to a large-scale chromosomal rearrangement in the coleoid ancestor that resulted in highly modified karyotypes, followed by lineage-specific fusions, translocations, and repeat expansions. How these events have shaped gene regulatory patterns underlying the evolution of coleoid innovations, including their large and elaborately structured nervous systems, novel organs, and complex behaviours, remains poorly understood. To address this, we integrate Micro-C, RNA-seq, and ATAC-seq across multiple coleoid species, developmental stages, and tissues. We find that while topological compartments are broadly conserved, hundreds of chromatin loops are species- and context-specific, with distinct regulation signatures and dynamic expression profiles. CRISPR-Cas9 knockout of a putative regulatory sequence within a conserved region demonstrates the role of loops in neural development and the prevalence of long-range, inter-compartmental interactions. We propose that differential evolutionary constraints across the coleoid 3D genome allow macroevolutionary processes to shape genome topology in distinct ways, facilitating the emergence of novel regulatory entanglements and ultimately contributing to the evolution and maintenance of complex traits in coleoids.
The general inorganic nature of traditional selection theory (based on differential growth between any two systems) is pointed out, wherefrom it follows that this theory cannot provide explanations for the characteristics of organic evolution. Specific biophysical aspects enter with the complexity of macro-molecules: vital physical conditions for the perpetuation of the system, irrevocable extinction (= death) and random change leading to novelty, are the result of 'complexity per se'. Further biophysical properties are a direct function of the pathway along which random mutation in nucleic acids is converted into continuous protein - (specifically enzyme) - function, from there into organismic phenotype with fitness components which may, or may not, correspond to identifiable structural units in DNA. The general machine-like properties of enzymes, in that there is no additive relationship between structural (amino acid) composition and functional output, is discussed in more detail. The continuous growth functions of molecular concentrations, directed by enzyme turnover, determine simple laws of growth and morphogenesis in the organic hierarchy and thus of phenotype. Thus, the combined effect of DNA-structure and of environmental parameters (temperature, pressure, pH, etc.) on protein function determines ultimately the actual phenotype and hence, quality and intensity of genotypic selection.
Retrons are bacterial genetic elements encoding a specialized reverse transcriptase (RT) that synthesizes multicopy single-stranded DNA and are increasingly recognized as components of bacterial anti-phage defense systems. However, their diversity and ecological distribution across large-scale genomic resources remain poorly characterized. Here, we surveyed retron RTs across the SPIRE representative metagenome collection, a non-redundant, species-level data set spanning diverse microbial habitats. Using a curated panel of type-specific hidden Markov models, we identified retrons representing all canonical types together with additional divergent lineages. Retron distribution showed strong taxonomic and ecological structuring, with some groups restricted to specific bacterial phyla, whereas others were broadly distributed across environmental categories. Systematic novelty assessment identified two candidate type XI-like lineages, TXI_C2like and TXI_noncan_h, characterized by protease-independent architectures and distinct accessory modules associated with WYL- and DnaB_C-containing proteins, respectively. De novo covariance-based analyses further identified candidate msr/msd-like non-coding RNA structures in both lineages, supporting conservation of the canonical RT-ncRNA organizational framework despite extensive sequence divergence. Together, these findings expand the known diversity of retron systems and identify type XI-like retrons as a dynamic and previously underexplored evolutionary group.IMPORTANCERetrons are bacterial genetic elements that are increasingly exploited as programmable tools for genome editing, molecular recording, and biosensing in addition to their natural role in anti-phage defense. Despite this growing biotechnological interest, the true diversity of retrons across the bacterial world has remained largely unmapped. By mining a resource of over 100,000 processed microbial metagenomes, we uncovered thousands of retron sequences spanning known types as well as previously unrecognized lineages and found that their distribution is strongly shaped by both bacterial taxonomy and ecological niche. Among these, we identified two candidate new lineages related to type XI retrons that lack the protease domain typical of this group but instead carry distinct accessory proteins, expanding the known architectural diversity of these systems. These findings broaden the catalog of retron diversity available for functional characterization and biotechnological engineering and provide a framework for prioritizing candidate lineages for future experimental validation.
Key innovations open ecological opportunities and can redirect evolutionary trajectories. In spiny-finned fishes, the pelvic suction cup-a fused adhesive structure formed from the pelvic fins and supported by a modified girdle-appears to be one such trait. Using a novel 960-species phylogeny spanning 940 exons and 67 newly sequenced snailfish genomes, we show that the suction cup evolved independently three times across lineages separated by over 100 million years. By enabling adhesion in high-energy habitats such as tide pools and waterfalls, the suction cup set the stage for body depression and accompanying shifts in scales, teeth, and clade-specific ecofunctional profiles. Comparative analyses reveal convergence in a distinctive region of morphospace and body-shape evolution accelerated two- to fivefold. Diversification analyses uncover heterogeneous but elevated rates, with a clear burst in rock-climbing gobies associated with suction cup evolution. By opening novel habitats and fostering phenotypic novelty, the suction cup emerges as a key innovation that reshaped spiny-finned fish evolution.
Neophobia, or aversion to novelty, is important for adaptability and survival as it influences the ways in which animals navigate risk and interact with their environments. Across individuals, species and other taxonomic levels, neophobia is known to vary considerably, but our understanding of the wider ecological drivers of neophobia is hampered by a lack of comparative multispecies studies using standardized methods. Here, we utilized the ManyBirds Project, a Big Team Science large-scale collaborative open science framework, to pool efforts and resources of 129 collaborators at 77 institutions from 24 countries worldwide across six continents. We examined both difference scores (between novel object test and control conditions) and raw data of latency to touch familiar food in the presence (test) and absence (control) of a novel object among 1,439 subjects from 136 bird species across 25 taxonomic orders incorporating lab, field, and zoo sites. We first demonstrated that consistent differences in neophobia existed among individuals, among species, and among other taxonomic levels in our dataset, rejecting the null hypothesis that neophobia is highly plastic at all taxonomic levels with no evidence for evolutionary divergence. We then tested for effects of ecological factors on neophobia, including diet, sociality, habitat, and range, while accounting for phylogeny. We found that (i) species with more specialist diets were more neophobic than those with more generalist diets, providing support for the Neophobia Threshold Hypothesis; (ii) migratory species were also more neophobic than nonmigratory species, which supports the Dangerous Niche Hypothesis. Our study shows that the evolution of avian neophobia has been shaped by ecological drivers and demonstrates the potential of Big Team Science to advance our understanding of animal behavior.
Enterococci appear to have originated in the guts of early terrestrializing arthropods and invertebrates over 425 million years ago-hosts that are now highly diverse and widespread in nature today. Yet most knowledge of the genus comes from human infection-associated lineages with genomes swollen by the recent accretion of foreign DNA conveyed by mobile elements. Because invertebrates dominate terrestrial animal diversity and biomass, they would be predicted to constitute a major but little-explored reservoir of enterococcal diversity. We therefore systematically examined Enterococcus association and species diversification in invertebrate hosts of the comparatively natural, isolated, but well-characterized environment of the Azorean island of Terceira. Over 100 invertebrate specimens were examined for associated enterococci, which were taxonomically classified by whole-genome sequencing. Supporting the existence of a large pool of uncharacterized enterococci and Enterococcus-adapted genes, 40% (eight of 20) of the Enterococcus species identified were either undescribed, including four candidate new species described here, or very recently discovered. In contrast, control isolates from vertebrates were exclusively of known species typical of sampling elsewhere, discounting geographic isolation as a main driver of the novelty observed. Further, because of the abundance of E. casseliflavus and E. flavescens in this collection, we obtained the resolution necessary to quantify the divergence and decipher the drivers of speciation in the controversial division between these naturally vancomycin-resistant species. These findings provide robust support for the existence of a large pool of new species and unexplored adaptive traits in invertebrate-associated enterococci-diverse environmental survival traits optimized for expression in an enterococcal background, and well positioned for transmission into human-associated enterococcal strains.IMPORTANCEEnterococci are auxotrophic gut-associated bacteria that co-evolved with their terrestrial hosts over many eons. In the last 75 years-the "antibiotic era"-E. faecalis and E. faecium gained genes for antibiotic resistance and enhanced virulence, emerging as leading causes of multidrug-resistant infection. Little is known about the source of those genes or the pathway by which they entered human-associated strains. A recent global survey suggested a potentially large repository of uncharacterized genetic diversity in the enterococci of invertebrates. We directly tested this prospect by examining enterococci of invertebrate hosts in a largely natural and pastoral environment. Our findings provide clear evidence that invertebrates naturally harbor vast unexplored enterococcal diversity. Moreover, associations are likely driven by intrinsic host selection factors rather than geographic isolation. This expands our knowledge of Enterococcus biodiversity, including the identification of four novel species, identifying a vast reservoir of enterococcal genes available to species that colonize and infect humans.
De novo genes, which originate from noncoding DNA, are known to have a high rate of turnover over short evolutionary timescales, such as within a species. Thus, their expression is often lineage- or genetic background-specific. However, little is known about their levels and breadth of expression as populations of a species diverge. In this study, we utilized publicly available RNA-seq data to examine the expression of newly evolved open reading frames (neORFs) in comparison to non- and protein-coding genes in Drosophila melanogaster populations from the derived species range in Europe and the ancestral range in sub-Saharan Africa. Our datasets included two adult tissue types as well as whole bodies at two temperatures for both sexes and three larval/prepupal developmental stages in a single tissue and sex, which allowed us to examine neORF expression and divergence across multiple sample types as well as sex and population. We detected a relatively large proportion (approximately 50%) of annotated neORFs as expressed in the population samples, with neORFs often showing greater expression divergence between populations than non- or protein-coding genes. However, differential expression of neORFs between populations tended to occur in a sample type-specific manner. On the other hand, neORFs displayed less sex-biased expression than the other two gene classes, with the majority of sex-biased neORFs detected in whole bodies, which may be attributable to the presence of the gonads. We also found that neORFs shared among multiple lines in the original set of inbred lines in which they were first detected were more likely to be both expressed and differentially expressed in the new population samples, suggesting that neORFs at a higher frequency (i.e. present in more individuals) within a species are more likely to be functional.