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Dornburg, A.

Publications and source records attributed to Dornburg, A..

At least 19 recordsLinked to original sources

Early Partitioning of Structural Paralog Diversity Shapes Immune Evolution Across Habitat Transitions in Gobiiform Fishes

Habitat transitions expose species lineages to novel pathogen regimes and are often hypothesized to drive adaptive diversification of immune gene families. However, the temporal association between gene family diversification and ecological change remains unresolved. To gain deeper insight into the relationship between the diversification of species and the evolution of their immune system, we investigated the evolutionary history of Toll-like receptors (TLRs) across Gobiiformes, a clade characterized by repeated transitions across aquatic and amphibious environments. TLRs are well-studied membrane-bound pattern recognition receptors that play crucial roles in detecting pathogens and immune activation. Phylogenomic, structural, and sequence analyses reveal that a major expansion of TLR22 predates many ecological transitions, with early paralog diversification partitioning receptor architectures into distinct structural regimes that persist across lineages. Subsequent evolution is concentrated in the extracellular ligand-binding, leucine-rich repeat (LRR) domains, where localized sequence and structural variation enables likely functional tuning without major architectural innovation. These results indicate that ecological transitions do not require repeated evolution of new immune receptor forms, but can instead be facilitated by reconfiguration of pre-existing immunogenetic diversity. These findings raise the possibility that expansions of immune gene families occurring early in a clades evolutionary history may commonly persist and subsequently act as substrates for evolutionary responses to environmental change.

evolutionary biology↗

Genomic Distortion of Jawed Vertebrate Phylogeny

Reconstructing patterns of evolution requires understanding the interrelationships of species, yet evolutionary relationships that defy resolution and calibration in time are commonplace across the Tree of Life. Here, we investigate the dynamics of temporal and topological uncertainty by generating a phylogeny of jawed vertebrates using 1105 exonic loci sampled for 540 species spanning all major orders and most families of gnathostomes. Across loci and DNA sequence sites, we observe rapid reductions in statistical support for the monophyly of jawed vertebrate clades that originated around the Cretaceous-Paleogene mass extinction. Phylogenetic signal was scrambled to different degrees during rapid successive divergences in multiple unrelated jawed vertebrate lineages that radiated in this interval, including birds, snakes, placental mammals, and acanthomorph fishes. In addition to showing that particular events have modified phylogenetic signal across the same loci in distantly related vertebrate clades, we also demonstrate how rates of genomic evolution affect our ability to infer the timescale of vertebrate evolution. By testing how the inclusion of lineages of ray-finned fishes with very fast and slow rates of molecular evolution changes inferences of the vertebrate evolutionary timescale, we show that the deepest divergences in ray-finned fishes may be impossible to accurately infer using sequence data and calibrations from a limited fossil record. These results hint at the macroevolutionary realities underlying topological and divergence time uncertainty across evolutionary trees.

evolutionary biology↗

Signal, noise, and bias in phylogenetic inference:potential and limits to the resolution of phylogenetic trees in the phylogenomic era

Phylogenomic datasets assembled to resolve the Tree of Life now routinely span thousands of loci comprising millions of characters. Yet the persistence of incongruent topologies across such datasets reveals a fundamental truth of phylogenetics: not all data are equally informative. Here we derive analytical approaches that predict the relative impacts of phylogenetic signal, stochastic noise, and systematic bias on phylogenetic inference. We show that these three components exhibit divergent scaling properties with character sampling: signal and bias accumulate linearly, while noise accumulates nonlinearly with a concave trajectory. For some phylogenetic problems, substantial amounts of phylogenetic noise may eventually be overwhelmed by signal. For other phylogenetic problems--especially those involving deep divergences, short internodes, or constrained character-state space--the slope of signal accumulation can be so shallow that even signal from genome-scale data may never practically exceed noise. Moreover, linear accumulation of phylogenetic bias can in principle continuously overwhelm accumulation of signal at a lower slope with additional characters, regardless of dataset size. Applying our theory to empirical datasets, we show that anchored hybrid enrichment and ultraconserved element loci, like any loci, can exhibit signal that is overwhelmed by noise, and that character acquisition biases in some loci can further confound inference. Given the pervasive nature of incongruence in the phylogenomic era, our work provides a theoretical foundation for understanding the limits of inference, improving experimental design, and guiding efficient and accurate resolution of the Tree of Life.

evolutionary biology↗

Rapid and repeated evolution of the pigmentation patterns in reef fishes

Pigmentation patterns are integral to animal biology1-3 and uncovering the mechanisms driving their diversification is essential for determining the evolutionary principles that shape this fundamental aspect of biodiversity4-7. Coral reef fishes are particularly notable for their extraordinary pattern diversity, ranging from simple spots and stripes to intricate, maze-like designs. Despite over a century of investigation, the evolutionary processes that govern the diversification of these pigmentation patterns remain one of the most persistent unresolved questions in evolutionary biology. Here, we investigate the relationship between pattern diversity, species richness, and geography across six iconic families of pattern-diverse coral reef fishes. Utilizing time-calibrated phylogenies, we reveal constant disparity of pigmentation patterns across globally variable reef fish communities8. We find strong evidence for a positive correlation between pattern diversity and species richness, with a high divergence of pigmentation patterns in sympatry that highlights the role of these patterns in speciation and phenotypic differentiation. Moreover, our findings support the stages model of adaptive radiation9, revealing that most pigmentation pattern diversity has emerged in evolutionary history. These results demonstrate that the evolutionary history of pigmentation patterns in reef fishes is characterized by a combination of rapid and constrained phenotypic diversification that has likely played a crucial role in their speciation dynamics.

evolutionary biology↗

Holostean genomes reveal evolutionary novelty in the vertebrate immunoproteasome that have implications for MHCI function

Holosteans (gars and bowfins) have emerged as valuable models for understanding early vertebrate evolution, offering insights into diverse topics ranging from genomic architecture to molecular processes. These lineages also exhibit unusual features in their immune response, combining molecular elements seen in both tetrapods and ray-finned fishes. However, the immune repertoire of holosteans remains relatively unexplored. Here, we investigate the evolution of PSMB8, a core component of the immunoproteasome responsible for cleaving intracellular proteins into peptides for presentation by MHC class I molecules. We identify two holostean PSMB8 types--S type and K type--that are unique among vertebrates. These types likely cause significant biochemical changes to the S1 binding pocket involved in antigen cleavage which could result in the presentation of novel peptides by MHC class I. Integrating comparative analyses across major ray-finned fish lineages demonstrates that bowfins and gars independently evolved the PSMB8 S type within separate PSMB8 paralog lineages, while the PSMB8-K type is an evolutionary novelty found only in gars. Our results provide new perspectives into PSMB8 haplotypes and their role in peptide antigen processing, offering unique insights into the molecular evolution of the vertebrate immunity and antigen presentation.

evolutionary biology↗

Cenozoic evolutionary history obscures the Mesozoic origins of acanthopterygian fishes

Sister lineage comparisons provide a valuable tool for understanding evolutionary origins of species-rich clades. Percomorpha, comprising over 18,900 species, represents one of the most species-rich vertebrate clades. However, the phylogenetic resolution of its sister lineage remains unclear, obscuring whether contrasts in histories of diversification provide insights into the factors that gave rise to this clades diversity. Using 887 ultraconserved element loci and Sanger-sequenced nuclear genes, we resolve the phylogenetic relationships of the three closest relatives of Percomorpha-the roughies, flashlightfishes, porcupinefishes and fangtooths (Trachichthyiformes), the squirrelfishes and soldierfishes (Holocentridae), and the whalefishes, bigscales, and alfonsinos (Berycoidei)-and the placement of percomorphs among them. Contrary to expectations from the fossil record, we demonstrate that living lineages of Berycoidei, Holocentridae, and Trachichthyiformes all diversified after the Cretaceous-Paleogene mass extinction. Our findings show that multiple clades in Trachichthyiformes and Berycoidei independently colonized deep ocean habitats during the climatically unstable Eocene and Oligocene and shallow-water reefs during the extensive hotspot migration and faunal turnover of the Early Miocene. Due to their complex evolutionary history, the closest relatives of Percomorpha are not ideal for understanding the origins of this exceptionally species-rich clade.

evolutionary biology↗

Reproductive innovation enabled radiation in the deep sea during an ecological crisis

Major ecological transitions are thought to fuel evolutionary radiations, but whether they are contingent on the evolution of certain traits is unclear. We show that the rapid ecological transition of anglerfishes into pelagic habitats during a period of major global warming coincided with the origins of sexual parasitism, in which male anglerfishes temporarily attach or permanently fuse to females to mate. A phylogenomic reconstruction of the evolutionary history of anglerfishes provides a strong inference for the convergent evolution of permanently-fusing deep-sea anglerfishes and their degenerate immune genes. Our results support that sexual parasitism was enabled by the degeneration of adaptive immunity and ancestral sexual size dimorphism. The combination of these traits facilitated the transition of pelagic anglerfishes into novel ecologies available in the deep open oceans after evolving from benthic ancestors. These results show how seemingly unrelated physiological and reproductive traits interact synergistically to drive evolutionary radiation in novel environments.

evolutionary biology↗

Investigating the impact of whole genome duplication on transposable element evolution in ray-finned fishes

Transposable elements (TEs) can make up more than 50% of any given vertebrates genome, with substantial variability in TE composition among lineages. TE variation is often linked to changes in gene regulation, genome size, and speciation. However, the role that genome duplication events have played in generating abrupt shifts in the composition of the mobilome over macroevolutionary timescales remains unclear. We investigated the degree to which the teleost genome duplication (TGD) shaped the diversification trajectory of the ray-finned fish mobilome. We integrate a new high coverage genome of Polypterus bichir with data from over 100 publicly available actinopterygian genomes to assess the macroevolutionary implications of genome duplication events on TE evolution. Our results provide no evidence for a substantial shift in mobilome composition following the TGD event. Instead, the diversity of the actinopterygian mobilome appears to have been shaped by a history of lineage specific shifts in composition that are not correlated with commonly evoked drivers of diversification such as body size, water column usage, or latitude. Collectively, these results provide a new perspective on the early diversification of the actinopterygian mobilome and suggest that historic ploidy events may not necessarily catalyze bursts of TE diversification and innovation.

bioinformatics↗

Purifying selection and adaptive evolution proximate to the zoonosis of SARS-CoV-1 and SARS-CoV-2

Over the past two decades the pace of spillovers from animal viruses to humans has accelerated, with COVID-19 becoming the most deadly zoonotic disease in living memory. Prior to zoonosis, it is conceivable that the virus might largely be subjected to purifying selection, requiring no additional selective changes for successful zoonotic transmission. Alternatively, selective changes occurring in the reservoir species may coincidentally preadapt the virus for human-to-human transmission, facilitating spread upon cross-species exposure. Here we quantify changes in the genomes of SARS-CoV-2 and SARS-CoV-1 proximate to zoonosis to evaluate the selection pressures acting on the viruses. Application of molecular-evolutionary and population-genetic approaches to quantify site-specific selection within both SARS-CoV genomes revealed strong purifying selection across many genes at the time of zoonosis. Even in the viral surface-protein Spike that has been fast-evolving in humans, there is little evidence of positive selection proximate to zoonosis. Nevertheless, in SARS-CoV-2, NSP12, a core protein for viral replication, exhibited a region under adaptive selection proximate to zoonosis. Furthermore, in both SARS-CoV-1 and SARS-CoV-2, regions of adaptive selection proximate to zoonosis were found in ORF7a, a putative Major Histocompatibility Complex modulatory gene. These findings suggest that these replication and immunomodulatory proteins have played a previously underappreciated role in the adaptation of SARS coronaviruses to human hosts.

evolutionary biology↗

Ancient Fish Lineages Illuminate Toll-Like Receptor Diversification in Early Vertebrate Evolution

Since its initial discovery over 50 years ago, understanding the evolution of the vertebrate adaptive immune response has been a major area of research focus for comparative geneticists. However, how the evolutionary novelty of an adaptive immune response impacted the diversity of receptors associated with the innate immune response has received considerably less attention until recently. Here we investigate the diversification of vertebrate Toll-like receptors (TLRs), one of the most ancient and well conserved innate immune receptor families found across the Tree of Life, integrating genomic data that represent all major vertebrate lineages with new transcriptomic data from Polypteriformes, the earliest diverging ray-finned fish lineage. Our analyses reveal TLR sequences that reflect the 6 major TLR subfamilies, TLR1, TLR3, TLR4, TLR5, TLR7, and TLR11, and also currently unnamed, yet phylogenetically distinct TLR clades. We additionally recover evidence for a pulse of gene gain coincident with the rise of the adaptive immune response in jawed vertebrates, followed by a period of rapid gene loss during the Cretaceous. These gene losses are primarily concentrated in marine teleost fish and synchronous with the mid Cretaceous anoxic event, a period of rapid extinction for marine species. Finally, we reveal a mismatch between phylogenetic placement and gene nomenclature for up to 50% of TLRs found in clades such as ray-finned fishes, cyclostomes, amphibians, and elasmobranchs. Collectively these results provide an unparalleled perspective of TLR diversity, and offer a ready framework for testing gene annotations in non-model species.

evolutionary biology↗

A chromosome level genome assembly of longnose gar, Lepisosteus osseus

Holosteans (gars and bowfins) represent the sister lineage to teleost fishes, the latter being a clade that comprises over half of all living vertebrates and includes important models for comparative genomics and human health. A major distinction between the evolutionary history of teleosts and holosteans is that all teleosts experienced a genome duplication event in their early evolutionary history. As holostean genomes did not undergo a round of genome duplication, they have been heralded as a means to bridge teleost models to other vertebrate genomes. However, only three species of holosteans have been genome sequenced to date and sequencing of more species is needed to fill sequence sampling gaps and provide a broader comparative basis for understanding holostean genome evolution. Here we report the first high quality reference genome assembly and annotation of the longnose gar (Lepisosteus osseus). Our final assembly consists of 22,709 scaffolds with a total length of 945 bp with contig N50 of 116.6 kb. Using BRAKER2, we annotated a total of 30,068 genes. Analysis of the repetitive regions of the genome reveals the genome to contain 29.1% transposable elements, and the longnose gar to be the only other known vertebrate outside of the spotted gar to contain CR1, L2, Rex1, and Babar. These results highlight the potential utility of holostean genomes for understanding the evolution of vertebrate repetitive elements and provide a critical reference for comparative genomic studies utilizing ray-finned fish models. SignificanceOver half of all living vertebrates are teleost fishes, including numerous experimental models such as zebrafish (Danio rerio) and medaka (Oryzias latipes). However, translating research in teleost models to other organisms such as humans is often challenged by the fact that teleosts experienced a genome duplication event in their early evolutionary history. Recent genome sequencing of three holosteans, the sister lineage to teleosts that did not experience a genome duplication event, has revealed these taxa to be critical for linking homologs between teleosts and other vertebrates. Sequencing of holostean genomes remains limited, thereby impeding further comparative genomic studies. Here we fill this sampling gap through the genomic sequencing of the longnose gar (Lepisosteus osseus). This annotated reference genome will provide a useful resource for a range of comparative genomic applications that span fields as diverse as immunogenetics, developmental biology, and the understanding of regulatory sequence evolution.

genomics↗

Molecular early burst associated with the diversification of birds at the K-Pg boundary

Complex patterns of genome and life-history evolution associated with the end-Cretaceous (K- Pg) mass extinction event limit our understanding of the early evolutionary history of crown group birds [1-9]. Here, we assess molecular heterogeneity across living birds using a technique enabling inferred sequence substitution models to transition across the history of a clade [10]. Our approach identifies distinct and contrasting regimes of molecular evolution across exons, introns, untranslated regions, and mitochondrial genomes. Up to fifteen shifts in the mode of avian molecular evolution map to rapidly diversifying clades near the Cretaceous-Palaeogene boundary, demonstrating a burst of genomic disparity early in the evolutionary history of crown birds [11-13]. Using simulation and machine learning techniques, we show that shifts in developmental mode [14] or adult body mass [4] best explain transitions in the mode of nucleotide substitution. These patterns are related, in turn, to macroevolutionary shifts in the allometric scaling relationship between basal metabolic rate and body mass [15, 16]. In agreement with theoretical predictions, this scaling relationship appears to have weakened across the end-Cretaceous transition. Overall, our study provides evidence that the Chicxulub bolide impact [17] triggered integrated patterns of evolution across avian genomes, physiology, and life history that structured the evolutionary potential of modern birds.

evolutionary biology↗

Decoupled spectral tuning and eye size diversification patterns in an Antarctic adaptive radiation

Evolutionary transitions in water column usage have played a major role in shaping ray-finned fish diversity. However, the extent to which vision-associated trait complexity and water column usage is coupled remains unclear. Here we investigate the relationship between depth niche, eye size, and the molecular basis of light detection across the Antarctic notothenioid adaptive radiation. Using a phylogenetic comparative framework, we integrate sequence analyses of opsin tuning sites with data on eye size and depth occupancy from over two decades of NOAA trawl-based surveys. We find a consistent signature of changes in tuning sites suggestive of shifts in their ability to detect lower wavelengths of light. These represent repeated instances of independent tuning site changes across the notothenioid phylogeny that are generally not associated with habitat depth or species eye size. We further reveal an acceleration in the rate of eye size diversification nearly 20 million years after the initial radiation that has manifested in high levels of eye size divergence among closely related taxa. Collectively, our results strongly support a decoupling of the diversification dynamics between opsin tuning sites, eye size and depth, providing a new perspective of the evolution of the visual system in this iconic adaptive radiation.

evolutionary biology↗

A highly diverse set of novel immunoglobulin-like transcript (NILT) genes in zebrafish indicates a wide range of functions with complex relationships to mammalian receptors

Multiple novel immunoglobulin-like transcripts (NILTs) have been identified from salmon, trout and carp. NILTs typically encode activating or inhibitory transmembrane receptors with extracellular immunoglobulin (Ig) domains. Although predicted to provide immune recognition in ray-finned fish, we currently lack a definitive framework of NILT diversity, thereby limiting our predictions for their evolutionary origin and function. In order to better understand the diversity of NILTs and their possible roles in immune function, we identified five NILT loci in the Atlantic salmon (Salmo salar) genome, defined 86 NILT Ig domains within a 3 Mbp region of zebrafish (Danio rerio) chromosome 1, and described 41 NILT Ig domains as part of an alternative haplotype for this same genomic region. We then identified transcripts encoded by 43 different NILT genes which reflect an unprecedented diversity of Ig domain sequences and combinations for a family of non-recombining receptors within a single species. Zebrafish NILTs include a sole putative activating receptor but extensive inhibitory and secreted forms as well as membrane-bound forms with no known signaling motifs. These results reveal a higher level of genetic complexity, interindividual variation and sequence diversity for NILTs than previously described, suggesting that this gene family likely plays multiple roles in host immunity.

immunology↗

Periodic Environmental Disturbance Drives Repeated Ecomorphological Diversification in an Adaptive Radiation of Antarctic Fishes

The ecological theory of adaptive radiation has profoundly shaped our conceptualization of the rules that govern diversification. However, while many radiations follow classic early burst patterns of diversification as they fill ecological space, the longer-term fates of these radiations depend on many factors, such as climatic stability. In systems with periodic disturbances, species-rich clades can contain nested adaptive radiations of subclades with their own distinct diversification histories, and how adaptive radiation theory applies in these cases is less clear. Here, we investigated patterns of ecological and phenotypic diversification within two iterative adaptive radiations of cryonotothenioid fishes in Antarcticas Southern Ocean: crocodile icefishes and notoperches. For both clades, we observe evidence of repeated diversification into disparate regions of trait space between closely related taxa and into overlapping regions of trait space between distantly related taxa. We additionally find little evidence that patterns of ecological divergence are correlated with evolution of morphological disparity, suggesting that these axes of divergence may not be tightly linked. Finally, we reveal evidence of repeated convergence in sympatry that suggests niche complementarity. These findings reflect the dynamic history of Antarctic marine habitats, and may guide hypotheses of diversification dynamics in environments characterized by periodic disturbance.

evolutionary biology↗

Considering decoupled phenotypic diversification between ontogenetic phases in macroevolution: An example using Triggerfishes (Balistidae)

Across the Tree of Life, most studies of phenotypic disparity and diversification have been restricted to adult organisms. However, many lineages have distinct ontogenetic phases that do not reflect the same traits as their adult forms. Non-adult disparity patterns are particularly important to consider for coastal ray-finned fishes, which often have juvenile phases with distinct phenotypes. These juvenile forms are often associated with sheltered nursery environments, with phenotypic shifts between adults and juvenile stages that are readily apparent in locomotor morphology. However, whether this ontogenetic variation in locomotor morphology reflects a decoupling of diversification dynamics between life stages remains unknown. Here we investigate the evolutionary dynamics of locomotor morphology between adult and juvenile triggerfishes. Integrating a time-calibrated phylogenetic framework with geometric morphometric approaches and measurement data of fin aspect ratio and incidence, we reveal a mismatch between morphospace occupancy, the evolution of morphological disparity, and the tempo of trait evolution between life stages. Collectively, our results illuminate how the heterogeneity of morpho-functional adaptations can decouple the mode and tempo of morphological diversification between ontogenetic stages.

evolutionary biology↗

Prolonged morphological expansion of spiny-rayed fishes following the end-Cretaceous

Spiny-rayed fishes (Acanthomorpha) dominate modern marine habitats and comprise more than a quarter of all living vertebrate species1-3. It is believed that this dominance resulted from explosive lineage and phenotypic diversification coincident with the Cretaceous-Paleogene (K-Pg) mass-extinction event4. It remains unclear, however, if living acanthomorph diversity is the result of a punctuated burst or gradual accumulation of diversity following the K-Pg. We assess these hypotheses with a time-calibrated phylogeny inferred using ultraconserved elements from a sampling of species that represent over 91% of all acanthomorph families, as well as an extensive body shape dataset of extant species. Our results indicate that several million years after the end-Cretaceous, acanthomorphs underwent a prolonged and significant expansion of morphological disparity primarily driven by changes in body elongation, and that acanthomorph lineages containing the bulk of the living species diversity originated throughout the Cenozoic. These acanthomorph lineages radiated into distinct regions of morphospace and retained their iconic phenotypes, including a large group of laterally compressed reef fishes, fast-swimming open-ocean predators, bottom-dwelling flatfishes, seahorses, and pufferfishes. The evolutionary success of spiny-rayed fishes is the culmination of a post K-Pg adaptive radiation in which rates of lineage diversification were decoupled from periods of high phenotypic disparity.

evolutionary biology↗

Holosteans contextualize the role of the teleost genome duplication in promoting the rise of evolutionary novelties in the ray-finned fish innate immune system

Over 99% of ray-finned fishes (Actinopterygii) are teleosts, a clade that comprises half of all living vertebrates that have diversified across virtually all fresh and saltwater ecosystems. This ecological diversity raises the question of how the immunogenetic diversity required to persist under heterogeneous pathogen pressures evolved. The teleost genome duplication (TGD) has been hypothesized as the evolutionary event that provided the genomic substrate for rapid genomic evolution and innovation. However, studies of putative teleost-specific innate immune receptors have been largely limited to comparisons either among teleosts or between teleosts and distantly related vertebrate clades such as tetrapods. Here we describe and characterize the receptor diversity of two clustered innate immune gene families in the teleost sister lineage: Holostei (bowfin and gars). Using genomic and transcriptomic data, we provide a detailed investigation of the phylogenetic history and conserved synteny of gene clusters encoding diverse immunoglobulin domain-containing proteins (DICPs) and novel immune-type receptors (NITRs). These data demonstrate an ancient linkage of DICPs to the major histocompatibility complex (MHC) and reveal an evolutionary origin of NITR variable-joining (VJ) exons that predate the TGD by at least 50 million years. Further characterizing the receptor diversity of Holostean DICPs and NITRs illuminates a sequence diversity that rivals the diversity of these innate immune receptor families in many teleosts. Taken together, our findings provide important historical context for the evolution of these gene families that challenge prevailing expectations concerning the consequences of the TGD during actinopterygiian evolution.

immunology↗