Biology subjects

Oakley, T. H.

Publications and source records attributed to Oakley, T. H..

17 recordsLinked to original sources

bioRxiv2026

Diel metabolic variation and the energetic demands of courtship in bioluminescent Photeros ostracods

The energetic demands of courtship are central to sexual selection, but their magnitude and temporal variation remain poorly quantified in many signalling systems. We used closed-chamber respirometry and low-light video analysis to estimate courtship-associated metabolic rates in males of the bioluminescent ostracod Photeros sp. "EGD." Low-activity metabolic rate varied strongly across the diel cycle: in small vessels that constrained movement, individually measured males consumed significantly more oxygen at night than during the day. We then compared oxygen consumption across vessels that differed in opportunities for movement and courtship. Metabolic rates were highest in large vessels that permitted bioluminescent courtship displays, intermediate in medium vessels that allowed swimming but not full displays, and lowest in small vessels that constrained movement. Oxygen consumption in large vessels at night was approximately 500% of small-vessel daytime rates, 280% of small-vessel nighttime rates, and 160% of medium-vessel nighttime rates. Because measurements integrated oxygen use over multi-hour intervals, these values represent time-averaged metabolic demand rather than instantaneous costs of individual light pulses or display trains. Video analyses suggested a positive association between signalling rate and oxygen consumption, although this relationship was not statistically supported in our large-vessel dataset, which had low statistical power. Together, these results show that male Photeros undergo strong diel shifts in metabolic state and that the whole-animal performance required to construct bioluminescent courtship displays may often impose substantial energetic demands. Summary statementMale sea fireflies show higher nighttime metabolic rates and increased oxygen consumption during courtship-associated activities, highlighting the physiological demands of producing complex bioluminescent displays.

physiology↗

bioRxiv2026

Competitive environment predicts weaponry in an intertidal sea anemone

Animal weapons are ecologically important traits that mediate contests over limiting resources and can strongly influence survival and reproduction. Weapon traits often exhibit substantial intraspecific morphological diversity, raising questions about the ecological drivers of this variation. Acrorhagi are weapons produced by sea anemones that are used in intraspecific territorial encounters. Although acrorhagial morphology varies widely within species, patterns of intraspecific variation remain poorly characterized, and the extent to which such variation reflects differences in local intraspecific competition is unclear. Here, we conduct morphometric analyses to characterize within-population variation and allometry in acrorhagial traits of the solitary anemone Anthopleura sola. We show that these traits covary with habitats differing in conspecific density. The number of acrorhagi scaled positively with body size, and individuals occupying a high-density habitat tended to possess more acrorhagi than did similar sized individuals from a low-density habitat. In addition, anemones from high-density habitats exhibited longer acrorhagial cnidae, a pattern that was not explained by differences in body size or acrorhagial density. Together, these results suggest that competitive context influences weapon-related traits at multiple levels of biological organization, potentially via phenotypic plasticity or selective processes. More broadly, our findings highlight how fine-scale ecological variation may contribute to the maintenance of trait diversity within and across species.

zoology↗

bioRxiv2026

Adaptive molecular convergence is pervasive across deep time and largely decoupled from phenotypic convergence

Researchers often infer evolutionary repeatability when selection scans implicate homologous genes in repeatedly evolved traits or ecologies. However, the causes and frequency of genome-scale molecular convergence remain unresolved, particularly over deep time. We show that adaptive molecular convergence-- excess convergence of nonsynonymous substitutions, consistent with positive selection--is pervasive across Medusozoa. Molecular convergence declines over time but persists among lineages separated by > 600 million years, exceeding null expectations based on random overlap. However, lineages sharing repeatedly evolved phenotypes (eyes, medusa loss, upright colonies) do not exhibit elevated molecular convergence relative to other comparisons. Instead, convergence is non-randomly distributed across genes and enriched for environment-facing functions, including metabolism, immunity, and xenobiotic processing, suggesting that widespread reuse of genes reflects multifaceted organism-environment interactions.

evolutionary biology↗

bioRxiv2025

Accessible and Robust Machine Learning Approaches to Improve the Opsin Genotype-Phenotype Map

Predicting phenotypes from genetic variation is a central challenge in biology. Linking genotypes and phenotypes using machine learning (ML) offers great promise, but its use is limited by poor accessibility, overestimated performance, and a "data-cliff"--a gap between abundant sequences and scarce functional measurements. To develop more robust methods for genotype-phenotype prediction, an outstanding model system is opsin genes, visual pigments with extensive phenotypic information that strongly influence animal spectral sensitivity. Here we advance ML characterization of the opsin genotype-phenotype map through four main contributions. First, we introduce the Opsin Phenotype Tool for Inference of Color Sensitivity (OPTICS), a user-friendly platform for predicting maximum wavelength sensitivity ({lambda}max) from amino-acid sequences. Second, we show that encoding sequences with amino-acid physicochemical properties improves predictive performance and reveals mechanistic relationships. Third, we develop Phylogenetically Weighted Cross-Validation (PW-CV), a method that accounts for non-independence among related sequences, providing more realistic assessments of model generalizability. Finally, we present the Mine-N-Match (MNM) pipeline, which systematically links published opsin sequences to compiled in-vivo {lambda}max data, expanding genotype-phenotype coverage and improving prediction, especially for invertebrate opsins with undersampled heterologous data. By integrating accessible software, biologically informed encoding, phylogeny-aware evaluation, and data harmonization, our framework improves confidence, accuracy, and interpretability of genotype-phenotype prediction. An accurate genotype-phenotype map allows simulating molecular evolution of function, reconstructing the history of visual phenotypes, designing functional proteins, and generating new hypotheses that can be tested with heterologous phenotyping.

bioinformatics↗

bioRxiv2025

Comparative analysis of convergent jellyfish eyes reveals extensive differences in expression of vision-related genes

Quantifying gene expression across convergent origins of traits clarifies the degree to which those traits arise from shared versus distinct genetic programs, revealing how gene re-use relates to the repeatability of evolution. Eyes are important traits that evolved in many distantly related lineages, including at least nine times within cnidarians. Here, we investigate gene expression in eye-bearing and non-visual tissues from three cnidarian species representing long-diverged lineages where eyes evolved convergently (Cubozoa, Scyphozoa, and Hydrozoa). We find gene expression in eye-bearing tissues to be mostly lineage-specific, with only a small proportion of genes having convergent expression across species. Nevertheless, all species express homologs of deeply conserved vision-related genes known from Bilateria, which likely reflects deep homology (parallel evolution across vast phylogenetic distances) of a metazoan phototransduction toolkit. A gene tree analysis of opsins--the prototypical animal photosensors--shows that convergent eyes recruited different opsin paralogs, with the potential exception of an opsin ortholog shared between scyphozoan and cubozoan eyes. Our results suggest that eyes have mostly lineage-specific patterns of gene expression, yet some key phototransduction components are repeatedly recruited across multiple independent eye origins in Medusozoa.

evolutionary biology↗

bioRxiv2025

Genome assembly of Bougainvillia cf. muscus (Cnidaria: Hydrozoa)

BackgroundAs one of just a handful of non-Bilaterian animal phyla, Cnidaria are key to understanding genome evolution across Metazoa. Despite their importance and diversity, the genomes of most species in the phylum are unsequenced, due in large part to difficulties cultivating them in a laboratory. Here, we present a genome sequence of Bougainvillia cf. mucus, a hydrozoan with four marginal bulbs each containing seven simple eyes (ocelli). This species appeared in our tanks from contamination. While we lacked sufficient samples for transcriptomic or functional studies, we were able to expand our knowledge of how the genome of this species compares to the few, better studied members of hydrozoans by investigating synteny to other cnidarians, repetitive element content, and phylogenetics and synteny of vision-related genes in this eyed species compared to eyeless relatives. ResultsThe genome sequence consists of 350 contigs with an N50 of 10 Mb, a total genome length of 375.328 Mb, a BUSCO score of 90.1%, and predicted protein coding genes totaling 46,431. We found a high degree of macrosynteny conservation with Hydra vulgaris and Hydractinia symbiolongicarpus. Repetitive elements make up 62% of this Bougainvillia genome. For vision-related genes, we identified 20 cnidarian opsins (cnidops) in Bougainvillia and found instances of gene duplication and loss in families associated with bilaterian eye development, phototransduction, and visual cycling. ConclusionsThis high-quality, contiguous genome in an eyed Hydrozoan will be a valuable resource for additional comparative genomic studies.

genomics↗

bioRxiv2024

Functional characterization of luciferase in a brittle star indicates parallel evolution influenced by genomic availability of haloalkane dehalogenase

Determining why convergent traits use distinct versus shared genetic components is crucial for understanding how evolutionary processes generate and sustain biodiversity. However, the factors dictating the genetic underpinnings of convergent traits remain incompletely understood. Here, we use heterologous protein expression, biochemical assays, and phylogenetic analyses to confirm the origin of a luciferase gene from haloalkane dehalogenases in the brittle star Amphiura filiformis. Through database searches and gene tree analyses, we also show a complex pattern of presence and absence of haloalkane dehalogenases across organismal genomes. These results first confirm parallel evolution across a vast phylogenetic distance, because octocorals like Renilla also use luciferase derived from haloalkane dehalogenases. This parallel evolution is surprising, even though previously hypothesized, because many organisms that also use coelenterazine as the bioluminescence substrate evolved completely distinct luciferases. The inability to detect haloalkane dehalogenases in the genomes of several bioluminescent groups suggests that the distribution of this gene family influences its recruitment as a luciferase. Together, our findings highlight how biochemical function and genomic availability help determine whether distinct or shared genetic components are used during the convergent evolution of traits like bioluminescence.

evolutionary biology↗

bioRxiv2024

Ancient secretory pathways contributed to the evolutionary origin of an ecologically impactful bioluminescence system

Evolutionary innovations in chemical secretion - such as the production of secondary metabolites, pheromones, and toxins - profoundly impact ecological interactions across a broad diversity of life. These secretory innovations may involve a "legacy-plus-innovation" mode of evolution, whereby new biochemical pathways are integrated with conserved secretory processes to create novel products. Among secretory innovations, bioluminescence is important because it evolved convergently many times to influence predator-prey interactions, while often producing courtship signals linked to increased rates of speciation. However, whether or not deeply conserved secretory genes are used in secretory bioluminescence remains unexplored. Here, we show that in the ostracod Vargula tsujii, the evolutionary novel c-luciferase gene is co-expressed with many conserved genes, including those related to toxin production and high-output protein secretion. Our results demonstrate that the legacy-plus-innovation mode of secretory evolution, previously applied to sensory modalities of olfaction, gustation, and nociception, also encompasses light-producing signals generated by bioluminescent secretions. This extension broadens the paradigm of secretory diversification to include not only chemical signals but also bioluminescent light as an important medium of ecological interaction and evolutionary innovation. Significance StatementAnimals produce an enormous diversity of secreted chemical products, like toxins and pheromones, with wide-ranging impacts on ecological interactions. Although a deeply conserved toolkit of secretory genes may often underlie chemical interactions mediated through smell, taste, and sensing pain, whether or not this evolutionary mode generalizes to sensing light is unknown. Here we show that a bioluminescence secretion system, which creates light for anti-predator and courtship interactions, also uses genes of a deeply conserved secretory toolkit. Therefore, secretory innovations may act through all sensory modalities by integrating conserved genes with novel biosynthesis pathways, to serve as crucibles of evolutionary and ecological diversity.

evolutionary biology↗

bioRxiv2024

Discovering genotype-phenotype relationships with machine learning and the Visual Physiology Opsin Database (VPOD)

BackgroundPredicting phenotypes from genetic variation is foundational for fields as diverse as bioengineering and global change biology, highlighting the importance of efficient methods to predict gene functions. Linking genetic changes to phenotypic changes has been a goal of decades of experimental work, especially for some model gene families including light-sensitive opsin proteins. Opsins can be expressed in vitro to measure light absorption parameters, including {lambda}max - the wavelength of maximum absorbance - which strongly affects organismal phenotypes like color vision. Despite extensive research on opsins, the data remain dispersed, uncompiled, and often challenging to access, thereby precluding systematic and comprehensive analyses of the intricate relationships between genotype and phenotype. ResultsHere, we report a newly compiled database of all heterologously expressed opsin genes with {lambda}max phenotypes called the Visual Physiology Opsin Database (VPOD). VPOD_1.0 contains 864 unique opsin genotypes and corresponding {lambda}max phenotypes collected across all animals from 73 separate publications. We use VPOD data and deepBreaks to show regression-based machine learning (ML) models often reliably predict {lambda}max, account for non-additive effects of mutations on function, and identify functionally critical amino acid sites. ConclusionThe ability to reliably predict functions from gene sequences alone using ML will allow robust exploration of molecular-evolutionary patterns governing phenotype, will inform functional and evolutionary connections to an organisms ecological niche, and may be used more broadly for de-novo protein design. Together, our database, phenotype predictions, and model comparisons lay the groundwork for future research applicable to families of genes with quantifiable and comparable phenotypes. Key PointsO_LIWe introduce the Visual Physiology Opsin Database (VPOD_1.0), which includes 864 unique animal opsin genotypes and corresponding {lambda}max phenotypes from 73 separate publications. C_LIO_LIWe demonstrate that regression-based ML models can reliably predict {lambda}max from gene sequence alone, predict non-additive effects of mutations on function, and identify functionally critical amino acid sites. C_LIO_LIWe provide an approach that lays the groundwork for future robust exploration of molecular-evolutionary patterns governing phenotype, with potential broader applications to any family of genes with quantifiable and comparable phenotypes. C_LI

bioinformatics↗

bioRxiv2023

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

Individuals often employ simple rules that can emergently synchronise behaviour. Some collective behaviours are intuitively beneficial, but others like mate signalling in leks occur across taxa despite theoretical individual costs. Whether disparate instances of synchronous signalling are similarly organised is unknown, largely due to challenges observing many individuals simultaneously. Recording field collectives and ex situ playback experiments, we describe principles of synchronous bioluminescent signals produced by marine ostracods (Crustacea; Luxorina) that seem behaviorally convergent with terrestrial fireflies, and with whom they last shared a common ancestor over 500 mya. Like synchronous fireflies, groups of signalling males use visual cues (intensity and duration of light) to decide when to signal. Individual ostracods also modulate their signal based on the distance to nearest neighbours. During peak darkness, luminescent "waves" of synchronous displays emerge and ripple across the sea floor every [~]60 seconds, but such periodicity decays within and between nights after the full moon. Our data reveal these bioluminescent aggregations are sensitive to both ecological and social light sources. Because the function of collective signals is difficult to dissect, evolutionary convergence, like in the synchronous visual displays of diverse arthropods, provides natural replicates to understand the generalities that produce emergent group behaviour.

animal behavior and cognition↗

bioRxiv2023

Predictable genetic recruitment for luciferin sulfation in the convergent evolution of bioluminescence

Genes from ancient families are sometimes involved in the convergent evolutionary origins of similar traits, even across vast phylogenetic distances. Sulfotransferases are an ancient family of enzymes that transfer sulfate from a donor to a wide variety of substrates, including probable roles in some bioluminescence systems. Here we demonstrate multiple sulfotransferases, highly expressed in light organs of the bioluminescent ostracod Vargula tsujii, transfer sulfate in vivo to the luciferin substrate, vargulin. We find luciferin sulfotransferases of ostracods are not orthologous to known luciferin sulfotransferases of fireflies or sea pansies; animals with distinct and convergently evolved bioluminescence systems compared to ostracods. Therefore, distantly related sulfotransferases were independently recruited at least three times, leading to parallel evolution of luciferin metabolism in three highly diverged organisms. Re-use of homologous genes is surprising in these bioluminescence systems because the other components, including luciferins and luciferases, are completely distinct. Whether convergently evolved traits incorporate ancient genes with similar functions or instead use distinct, often newer, genes may be constrained by how many genetic solutions exist for a particular function. When fewer solutions exist, as in genetic sulfation of small molecules, evolution may be more constrained to use the same genes time and again.

evolutionary biology↗

bioRxiv2022

A morphological basis for path dependent evolution of visual systems

Path dependence influences macroevolutionary predictability by constraining potential outcomes after stochastic evolutionary events. Although demonstrated in laboratory experiments, the basis of path dependence is difficult to demonstrate in natural systems because of a lack of independent replicates. Here we show two types of complex distributed visual systems each recently evolved twice within chiton mollusks, demonstrating rapid and path dependent evolution. The type of visual system a chiton lineage evolves is constrained by the number of openings for optic nerves in its shell plates: lineages with more openings evolve visual systems with thousands of eyespots, whereas those with fewer evolve visual systems with hundreds of shell eyes. These macroevolutionary outcomes shaped by path dependence are both deterministic and stochastic because possibilities are restricted yet not entirely predictable. One-Sentence SummaryMultiple convergent origins of visual systems show macroevolution of complex traits can be rapid and contingent upon pre-existing structures

evolutionary biology↗

bioRxiv2021

Transcriptome phylogenies support ancient evolutionary transitions in bioluminescence traits of cypridinid ostracods

Although the the diversity, beauty, and intricacy of sexually selected courtship displays command the attention of evolutionists, the longevity of these traits in deep time is poorly understood. Population-based theory suggests sexual selection could either lower or raise extinction risk, resulting in high or low persistence of lineages with sexually selected traits. Furthermore, empirical studies that directly estimate longevity of sexually selected traits are uncommon. Sexually selected signals - including bioluminescent courtship - originated multiple times during evolution, allowing empirical study of their longevity after careful phylogenetic and divergence time analyses. Here, we estimate the first transcriptome-based molecular phylogeny and divergence times of Cypridinidae. We report extreme longevity of bioluminescent courtship, a trait important in mate choice and probably under sexual selection. Our relaxed-clock estimates of divergence times coupled with stochastic character mapping show luminous courtship evolved only once in Cypridinidae in a Sub-Tribe we name Luxorina at least 151 Million Years Ago (Ma) from cypridinid ancestors that used bioluminescence only in anti-predator displays, defining a Tribe we name Luminini. This time-calibrated molecular phylogeny of cypridinids will serve as a foundation for integrative and comparative studies on the biochemistry, molecular evolution, courtship, diversification, and ecology of cypridinid bioluminescence. The persistence of luminous courtship for hundreds of millions of years indicates that rates of speciation within the group exceeded extinction risk, allowing for the persistence of a diverse clade of signalling species and that sexual selection did not cause rapid loss of associated traits.

evolutionary biology↗

bioRxiv2020

Molecular evolution of luciferase diversified bioluminescent signals in sea fireflies (Crustacea:Ostracoda:Cypridinidae)

Understanding the genetic causes of evolutionary diversification is challenging because differences across species are complex, often involving many genes. However, cases where single or few genetic loci affect a feature that varies dramatically across a radiation of species would provide tractable opportunities to understand the genetics of diversification. Here, we show the diversification of bioluminescent signals in cypridinid ostracods ("sea fireflies") to be strongly influenced by a single gene, cypridinid-luciferase. We find different evolutionary processes, including selection, drift, and constraint, each acted on c-luciferase at different times during evolutionary history and impacted different phenotypes, diversifying behavioral signals across species. In particular, some amino acid sites in c-luciferase evolved under episodic diversifying selection, and are associated significantly with phenotypic changes in both enzyme kinetics and color, which impact signals directly. We also find that multiple other amino acid positions in c-luciferase evolved neutrally or under purifying selection and may have impacted the variation of color of bioluminescent signals across genera. This work provides a rare glimpse into the genetic basis of diversification across many species, showing how multiple evolutionary processes may act at different times during a radiation of species to diversify phenotypes. These results indicate not only selection but also drift and constraint may be important evolutionary drivers of species diversification. Significance statementA hallmark of life is its astounding diversity. While we are beginning to understand the drivers of biodiversity, uncovering the genetic basis remains challenging. As such, how different molecular evolutionary processes act to diversify phenotypes is a major question in biology. Here we show a single gene to be important in a riotous diversity of fantastical behaviors - the bioluminescent signals of sea fireflies - allowing us to demonstrate multiple evolutionary forces including selection, drift, and constraint contributed to diversification. Our work highlights that not only selection but also neutral processes and constraint have each worked at different times to shape phenotypic diversity.

evolutionary biology↗

bioRxiv2019

Laboratory culture of the California Sea Firefly Vargula tsujii (Ostracoda: Cypridinidae): Developing a model system for the evolution of marine bioluminescence

Bioluminescence, or the production of light by living organisms via chemical reaction, is widespread across Metazoa. Culture of bioluminescent organisms from diverse taxonomic groups is important for determining the biosynthetic pathways of bioluminescent substrates, which may lead to new tools for biotechnology and biomedicine. Some bioluminescent groups may be cultured, including some cnidarians, ctenophores, and brittle stars, but those use luminescent substrates (luciferins) obtained from their diets, and therefore are not informative for determination of the biosynthethic pathways of the luciferins. Other groups, including terrestrial fireflies, do synthesize their own luciferin, but culturing them is difficult, and the biosynthetic pathway for firefly luciferin remains unclear. An additional independent origin of endogenous bioluminescence is found within ostracods from the family Cypridinidae, which use their luminescence for defense and, in Caribbean species, for courtship displays. Here, we report the first complete life cycle of a luminous ostracod (Vargula tsujii Kornicker & Baker, 1977, the California Sea Firefly) in the laboratory. We also describe the late-stage embryogenesis of Vargula tsujii and discuss the size classes of instar development. We find embryogenesis in V. tsujii ranges from 25-38 days, and this species appears to have five instar stages, consistent with ontogeny in other cypridinid lineages. We estimate a complete life cycle at 3-4 months. We also present the first complete mitochondrial genome for Vargula tsujii. Bringing a luminous ostracod into laboratory culture sets the stage for many potential avenues of study, including learning the biosynthetic pathway of cypridinid luciferin and genomic manipulation of an autogenic bioluminescent system.

developmental biology↗

bioRxiv2017

The genome sizes of ostracod crustaceans correlate with body size and phylogeny

Within animals a positive correlation between genome size and body size has been detected in several taxa but not in others, such that it remains unknown how pervasive this pattern may be. Here we provide another example of a positive relationship, in a group of crustaceans whose genome sizes have not previously been investigated. We analyze genome size estimates for 46 species across Class Ostracoda, including 29 new estimates made using Feulgen image analysis densitometry and flow cytometry. Genome sizes in this group range ~80-fold, a level of variability that is otherwise not seen in crustaceans with the exception of some malacostracan orders. We find a strong positive correlation between genome size and body size across all species, including after phylogenetic correction. We additionally detect evidence of XX/XO sex determination in all three species of myodocopids where male and female genome sizes were estimated. On average, genome sizes are larger but less variable in myodocopids than in podocopids, and marine ostracods have larger genomes than freshwater species, but this appears to be explained by phylogenetic inertia. The relationship between phylogeny, genome size, body size, and habitat is complex in this system, and will benefit from additional data collection across various habitats and ostracod taxa.

evolutionary biology↗

bioRxiv2017

Novelty by Furcation and Fusion: How tree-like is evolution?

Novelty and innovation are fundamental yet relatively understudied concepts in evolution. We may study novelty phylogenetically, with a key question of whether evolution occurs by tree-like branching, or through exchange of distantly related parts in processes akin to horizontal transfer. Here, I argue that except at the lowest levels of biological organization, evolution is not usually tree-like. Perfectly vertical inheritance, an assumption of evolutionary trees, requires simultaneous co-duplication of all the parts of a duplicating or speciating (which I collectively call 'furcating') biological feature. However, simultaneous co-duplication of many parts usually requires variational processes that are rare. Therefore, instead of being perfectly tree-like, evolution often involves events that incorporate or fuse more distantly related parts into new units during evolution, which herein I call 'fusion'. Exon shuffling, horizontal gene transfer, introgression and co-option are such fusion processes at different levels of organization. In addition to co-duplication, units under phylogenetic study must individuate (gaining evolutionary independence) before they can diverge. A lack of individuation erases evolutionary history, and provides another challenge to tree-like evolution. In particular, biological units in the same organism that are the products of development always share the same genome, perhaps making full individuation difficult. The ubiquity of processes that fuse distantly related parts or oppose individuation has wide ranging implications for the study of macroevolution. For one, the central metaphor of a tree of life will often be violated, to the point where we may need a different metaphor, such as economic public goods, or a web of life. Secondly, we may need to expand current models. For example, even under the prevailing model of cell-type evolution, the sister-cell-type model, a lack of complete individuation and evolution by co-option will often be involved in forming new cell-types. Finally, these processes highlight a need for an expansive toolkit for studying evolutionary history. Multivariate methods are particularly critical to discover co-variation, the hallmark of an absence of complete individuation. In addition to studying phylogenetic trees, we may often need to analyze and visualize phylogenetic networks. Even though furcation - the splitting and individuation of biological features - does happen, fusion of distant events is just as critical for the evolution of novelties, and must formally be incorporated into the metaphors, models, and visualization of evolutionary history.

evolutionary biology↗