Daryl A Taketa, Liviu Cengher, Delany Rodriguez, Adam D Langenbacher, Anthony W De Tomaso
Histocompatibility is the ability to discriminate between self and non-self tissues, and has been described in species throughout the metazoa. Despite its universal presence, histocompatibility genes utilized by different phyla are unique-those found in sponges, cnidarians, ascidians, and vertebrates are not orthologous. Thus, the origins of these sophisticated recognition systems, and any potential functional commonalities between them, are not understood. We are studying histocompatibility in the botryllid ascidians, members of the chordate subphylum, Tunicata, which provide a powerful model to understand both the origins and functional aspects of this process. Histocompatibility in the botryllids occurs at the tips of an extracorporeal vasculature that come into contact when two individuals grow into proximity. If compatible, the vessels will fuse, forming a parabiosis between the two individuals. If incompatible, the two vessels will reject-an inflammatory reaction that results in melanin scar formation at the point of contact, blocking anastomosis. Compatibility is determined by a single, highly polymorphic locus called the fuhc with the following rules: individuals that share one or both fuhc alleles will fuse, while those who share neither will reject. The fuhc locus encodes at least six proteins with known roles in allorecognition. One of these genes, called uncle fester, is necessary and sufficient to initiate the rejection response. Here, we report the existence of genotype-specific expression levels of uncle fester, differing by up to eight-fold at the mRNA-level, and that these expression levels are constant and maintained for the lifetime of an individual. We also found that these differences had functional consequences: the expression level of uncle fester correlated with the speed and severity of the rejection response. These findings support previous conclusions that uncle fester levels modulate the rejection response, and may be responsible for controlling the variation observed in the timing and intensity of the reaction. The maintenance of genotype specific expression of uncle fester is also evidence of an education process reminiscent of that which occurs in mammalian Natural Killer cells. In turn, this suggests that while histocompatibility receptors and ligands evolve via convergent evolution, they may utilize conserved intracellular machinery to interpret binding events at the cell surface.
{"title":"Genotype-specific Expression of Uncle Fester Suggests a Role in Allorecognition Education in a Basal Chordate.","authors":"Daryl A Taketa, Liviu Cengher, Delany Rodriguez, Adam D Langenbacher, Anthony W De Tomaso","doi":"10.1093/icb/icae107","DOIUrl":"10.1093/icb/icae107","url":null,"abstract":"<p><p>Histocompatibility is the ability to discriminate between self and non-self tissues, and has been described in species throughout the metazoa. Despite its universal presence, histocompatibility genes utilized by different phyla are unique-those found in sponges, cnidarians, ascidians, and vertebrates are not orthologous. Thus, the origins of these sophisticated recognition systems, and any potential functional commonalities between them, are not understood. We are studying histocompatibility in the botryllid ascidians, members of the chordate subphylum, Tunicata, which provide a powerful model to understand both the origins and functional aspects of this process. Histocompatibility in the botryllids occurs at the tips of an extracorporeal vasculature that come into contact when two individuals grow into proximity. If compatible, the vessels will fuse, forming a parabiosis between the two individuals. If incompatible, the two vessels will reject-an inflammatory reaction that results in melanin scar formation at the point of contact, blocking anastomosis. Compatibility is determined by a single, highly polymorphic locus called the fuhc with the following rules: individuals that share one or both fuhc alleles will fuse, while those who share neither will reject. The fuhc locus encodes at least six proteins with known roles in allorecognition. One of these genes, called uncle fester, is necessary and sufficient to initiate the rejection response. Here, we report the existence of genotype-specific expression levels of uncle fester, differing by up to eight-fold at the mRNA-level, and that these expression levels are constant and maintained for the lifetime of an individual. We also found that these differences had functional consequences: the expression level of uncle fester correlated with the speed and severity of the rejection response. These findings support previous conclusions that uncle fester levels modulate the rejection response, and may be responsible for controlling the variation observed in the timing and intensity of the reaction. The maintenance of genotype specific expression of uncle fester is also evidence of an education process reminiscent of that which occurs in mammalian Natural Killer cells. In turn, this suggests that while histocompatibility receptors and ligands evolve via convergent evolution, they may utilize conserved intracellular machinery to interpret binding events at the cell surface.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1269-1277"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579525/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565149","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Animals have evolved behavioral and morphological traits that allow them to respond to environmental challenges. However, these traits may have long-term consequences that could impact an animal's performance, fitness, and welfare. Several species in a group of the arachnid order of Opiliones release their legs voluntarily to escape predators. These animals use their legs for locomotion, sensation, and reproduction. Here, we first compile data across species in the suborder Eupnoi, showing that more than half of individuals are found missing legs. Then, we review recent work on the ultimate and proximate implications of leg loss in Opiliones. Field and laboratory experiments showed that leg loss (a) did not affect their survival or mating success and (b) compromised the kinematics and energetics of locomotion, but individuals recovered velocity and acceleration quickly. These findings demonstrate that these animals display robustness, that is, the ability to withstand and overcome the potential consequences of bodily damage. This may explain why leg loss is so prevalent in Opiliones. Additionally, we encourage researchers to consider expanding their hypotheses beyond traditional adaptationist and ableist lenses and incorporate a comprehensive examination of animal welfare when studying animals' responses to bodily damage. Finally, we highlight avenues for future research in Opiliones, namely assessing how individuals move in three-dimensional environments, the neural plasticity aiding recovery post-leg loss, applications for bio-inspired design, and evidence-based animal welfare measures.
{"title":"Robustness to Leg Loss in Opiliones: A Review and Framework Considerations for Future Research.","authors":"Ignacio Escalante, Shannon L O'Brien","doi":"10.1093/icb/icae051","DOIUrl":"10.1093/icb/icae051","url":null,"abstract":"<p><p>Animals have evolved behavioral and morphological traits that allow them to respond to environmental challenges. However, these traits may have long-term consequences that could impact an animal's performance, fitness, and welfare. Several species in a group of the arachnid order of Opiliones release their legs voluntarily to escape predators. These animals use their legs for locomotion, sensation, and reproduction. Here, we first compile data across species in the suborder Eupnoi, showing that more than half of individuals are found missing legs. Then, we review recent work on the ultimate and proximate implications of leg loss in Opiliones. Field and laboratory experiments showed that leg loss (a) did not affect their survival or mating success and (b) compromised the kinematics and energetics of locomotion, but individuals recovered velocity and acceleration quickly. These findings demonstrate that these animals display robustness, that is, the ability to withstand and overcome the potential consequences of bodily damage. This may explain why leg loss is so prevalent in Opiliones. Additionally, we encourage researchers to consider expanding their hypotheses beyond traditional adaptationist and ableist lenses and incorporate a comprehensive examination of animal welfare when studying animals' responses to bodily damage. Finally, we highlight avenues for future research in Opiliones, namely assessing how individuals move in three-dimensional environments, the neural plasticity aiding recovery post-leg loss, applications for bio-inspired design, and evidence-based animal welfare measures.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1338-1353"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141089379","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Whether walking, running, slithering, or flying, organisms display a remarkable ability to move through complex and uncertain environments. In particular, animals have evolved to cope with a host of uncertainties-both of internal and external origin-to maintain adequate performance in an ever-changing world. In this review, we present mathematical methods in engineering to highlight emerging principles of robust and adaptive control of organismal locomotion. Specifically, by drawing on the mathematical framework of control theory, we decompose the robust and adaptive hierarchical structure of locomotor control. We show how this decomposition along the robust-adaptive axis provides testable hypotheses to classify behavioral outcomes to perturbations. With a focus on studies in non-human animals, we contextualize recent findings along the robust-adaptive axis by emphasizing two broad classes of behaviors: (1) compensation to appendage loss and (2) image stabilization and fixation. Next, we attempt to map robust and adaptive control of locomotion across some animal groups and existing bio-inspired robots. Finally, we highlight exciting future directions and interdisciplinary collaborations that are needed to unravel principles of robust and adaptive locomotion.
{"title":"Moving in an Uncertain World: Robust and Adaptive Control of Locomotion from Organisms to Machine Intelligence.","authors":"Jean-Michel Mongeau, Yu Yang, Ignacio Escalante, Noah Cowan, Kaushik Jayaram","doi":"10.1093/icb/icae121","DOIUrl":"10.1093/icb/icae121","url":null,"abstract":"<p><p>Whether walking, running, slithering, or flying, organisms display a remarkable ability to move through complex and uncertain environments. In particular, animals have evolved to cope with a host of uncertainties-both of internal and external origin-to maintain adequate performance in an ever-changing world. In this review, we present mathematical methods in engineering to highlight emerging principles of robust and adaptive control of organismal locomotion. Specifically, by drawing on the mathematical framework of control theory, we decompose the robust and adaptive hierarchical structure of locomotor control. We show how this decomposition along the robust-adaptive axis provides testable hypotheses to classify behavioral outcomes to perturbations. With a focus on studies in non-human animals, we contextualize recent findings along the robust-adaptive axis by emphasizing two broad classes of behaviors: (1) compensation to appendage loss and (2) image stabilization and fixation. Next, we attempt to map robust and adaptive control of locomotion across some animal groups and existing bio-inspired robots. Finally, we highlight exciting future directions and interdisciplinary collaborations that are needed to unravel principles of robust and adaptive locomotion.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1390-1407"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579605/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141876694","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
A surprising insight from the advent of genomic sequencing was that many genes are deeply conserved during evolution. With a particular focus on genes that interact with light in animals, I explore the metaphor of genetic toolkits, which can be operationalized as lists of genes involved in a trait of interest. A fascinating observation is that genes of a toolkit are often used again and again during convergent evolution, sometimes across vast phylogenetic distances. Such a pattern in the evolution of toolkits requires three different stages: (i) origin, (ii) maintenance, and (iii) redeployment of the genes. The functional origins of toolkit genes might often be rooted in interactions with external environments. The origins of light interacting genes in particular may be tied to ancient responses to photo-oxidative stress, inspiring questions about the extent to which the evolution of other toolkits was also impacted by stress. Maintenance of genetic toolkits over long evolutionary timescales requires gene multifunctionality to prevent gene loss when a trait of interest is absent. Finally, the deployment of toolkit genes in convergently evolved traits like eyes sometimes involves the repeated use of similar, ancient genes yet other times involves different genes, specific to each convergent origin. How often a particular gene family is used time and again for the same function may depend on how many possible biological solutions are available. When few solutions exist and the genes are maintained, evolution may be constrained to use the same genes over and over. However, when many different solutions are possible, convergent evolution often takes multiple different paths. Therefore, a focus on genetic toolkits highlights the combination of legacy-plus-innovation that drives the evolution of biological diversity.
{"title":"Building, Maintaining, and (re-)Deploying Genetic Toolkits during Convergent Evolution.","authors":"Todd H Oakley","doi":"10.1093/icb/icae114","DOIUrl":"10.1093/icb/icae114","url":null,"abstract":"<p><p>A surprising insight from the advent of genomic sequencing was that many genes are deeply conserved during evolution. With a particular focus on genes that interact with light in animals, I explore the metaphor of genetic toolkits, which can be operationalized as lists of genes involved in a trait of interest. A fascinating observation is that genes of a toolkit are often used again and again during convergent evolution, sometimes across vast phylogenetic distances. Such a pattern in the evolution of toolkits requires three different stages: (i) origin, (ii) maintenance, and (iii) redeployment of the genes. The functional origins of toolkit genes might often be rooted in interactions with external environments. The origins of light interacting genes in particular may be tied to ancient responses to photo-oxidative stress, inspiring questions about the extent to which the evolution of other toolkits was also impacted by stress. Maintenance of genetic toolkits over long evolutionary timescales requires gene multifunctionality to prevent gene loss when a trait of interest is absent. Finally, the deployment of toolkit genes in convergently evolved traits like eyes sometimes involves the repeated use of similar, ancient genes yet other times involves different genes, specific to each convergent origin. How often a particular gene family is used time and again for the same function may depend on how many possible biological solutions are available. When few solutions exist and the genes are maintained, evolution may be constrained to use the same genes over and over. However, when many different solutions are possible, convergent evolution often takes multiple different paths. Therefore, a focus on genetic toolkits highlights the combination of legacy-plus-innovation that drives the evolution of biological diversity.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1505-1512"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141725125","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Harry Tuazon, Samuel David, Kenneth Ma, Saad Bhamla
We investigate how the Helobdella sp. freshwater leeches capture and consume Lumbriculus variegatus blackworms despite the blackworm's ultrafast helical swimming escape reflex and ability to form large tangled "blobs." We describe a spiral "entombment" predation strategy, where Helobdellid leeches latch onto blackworms with their anterior sucker and envelop them in a spiral cocoon. Quantitative analysis shows that larger leeches succeed more often in entombing prey, while longer worms tend to escape. The rate of spiral contraction correlates with entombment outcomes, with slower rates associated with success. These insights highlight the complex interactions between predator and prey in freshwater ecosystems, providing new perspectives on ecological adaptability and predator-prey dynamics.
{"title":"Leeches Predate on Fast-Escaping and Entangling Blackworms by Spiral Entombment.","authors":"Harry Tuazon, Samuel David, Kenneth Ma, Saad Bhamla","doi":"10.1093/icb/icae118","DOIUrl":"10.1093/icb/icae118","url":null,"abstract":"<p><p>We investigate how the Helobdella sp. freshwater leeches capture and consume Lumbriculus variegatus blackworms despite the blackworm's ultrafast helical swimming escape reflex and ability to form large tangled \"blobs.\" We describe a spiral \"entombment\" predation strategy, where Helobdellid leeches latch onto blackworms with their anterior sucker and envelop them in a spiral cocoon. Quantitative analysis shows that larger leeches succeed more often in entombing prey, while longer worms tend to escape. The rate of spiral contraction correlates with entombment outcomes, with slower rates associated with success. These insights highlight the complex interactions between predator and prey in freshwater ecosystems, providing new perspectives on ecological adaptability and predator-prey dynamics.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1408-1415"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579603/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141725126","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Phenotypic integration is often perceived as being able to produce convergent evolution in the absence of selection, but specific mechanisms for this process are lacking and a connection has never been empirically demonstrated. A new model of the effect of integration on convergence provides such a mechanism, along with other predictions about the influence of integration on evolutionary patterns. I use simulations and data from three empirical systems-turtle shells, characiform fish, and squirrel mandibles-to investigate the degree to which evolutionary integration is associated with high levels of convergent evolution. Levels of integration were varied in Brownian motion simulations and the resulting amounts of stochastic convergent evolution were quantified. Each empirical system was divided into modules, and the strength of integration, average amount of convergence, phenotypic disparity, and rate of evolution in each module were measured. Results from the simulations and from all three empirical systems converge on a common result: higher levels of phenotypic integration are indeed associated with higher levels of convergence. This is despite a lack of consistent association between the strength of phenotypic integration and evolutionary rate or disparity. The results here are only correlational. Further studies that more closely examine the influence of within-population drivers of evolutionary integration-for example, genetic or developmental integration-on convergence are required before it is possible to definitively establish when phenotypic integration can cause evolutionary convergence. Until then, however, the results of this study strongly suggest that phenotypic integration will often promote convergent evolution.
{"title":"Does Phenotypic Integration Promote Convergent Evolution?","authors":"C Tristan Stayton","doi":"10.1093/icb/icae041","DOIUrl":"10.1093/icb/icae041","url":null,"abstract":"<p><p>Phenotypic integration is often perceived as being able to produce convergent evolution in the absence of selection, but specific mechanisms for this process are lacking and a connection has never been empirically demonstrated. A new model of the effect of integration on convergence provides such a mechanism, along with other predictions about the influence of integration on evolutionary patterns. I use simulations and data from three empirical systems-turtle shells, characiform fish, and squirrel mandibles-to investigate the degree to which evolutionary integration is associated with high levels of convergent evolution. Levels of integration were varied in Brownian motion simulations and the resulting amounts of stochastic convergent evolution were quantified. Each empirical system was divided into modules, and the strength of integration, average amount of convergence, phenotypic disparity, and rate of evolution in each module were measured. Results from the simulations and from all three empirical systems converge on a common result: higher levels of phenotypic integration are indeed associated with higher levels of convergence. This is despite a lack of consistent association between the strength of phenotypic integration and evolutionary rate or disparity. The results here are only correlational. Further studies that more closely examine the influence of within-population drivers of evolutionary integration-for example, genetic or developmental integration-on convergence are required before it is possible to definitively establish when phenotypic integration can cause evolutionary convergence. Until then, however, the results of this study strongly suggest that phenotypic integration will often promote convergent evolution.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1484-1493"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141071620","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gregg W C Thomas, Patrick Gemmell, Subir B Shakya, Zhirui Hu, Jun S Liu, Timothy B Sackton, Scott V Edwards
Comparative genomics provides ample ways to study genome evolution and its relationship to phenotypic traits. By developing and testing alternate models of evolution throughout a phylogeny, one can estimate rates of molecular evolution along different lineages in a phylogeny and link these rates with observations in extant species, such as convergent phenotypes. Pipelines for such work can help identify when and where genomic changes may be associated with, or possibly influence, phenotypic traits. We recently developed a set of models called PhyloAcc, using a Bayesian framework to estimate rates of nucleotide substitution on different branches of a phylogenetic tree and evaluate their association with pre-defined or estimated phenotypic traits. PhyloAcc-ST and PhyloAcc-GT both allow users to define a priori a set of target lineages and then compare different models to identify loci accelerating in one or more target lineages. Whereas ST considers only one species tree across all input loci, GT considers alternate topologies for every locus. PhyloAcc-C simultaneously models molecular rates and rates of continuous trait evolution, allowing the user to ask whether the two are associated. Here, we describe these models and provide tips and workflows on how to prepare the input data and run PhyloAcc.
{"title":"Practical Guidance and Workflows for Identifying Fast Evolving Non-Coding Genomic Elements Using PhyloAcc.","authors":"Gregg W C Thomas, Patrick Gemmell, Subir B Shakya, Zhirui Hu, Jun S Liu, Timothy B Sackton, Scott V Edwards","doi":"10.1093/icb/icae056","DOIUrl":"10.1093/icb/icae056","url":null,"abstract":"<p><p>Comparative genomics provides ample ways to study genome evolution and its relationship to phenotypic traits. By developing and testing alternate models of evolution throughout a phylogeny, one can estimate rates of molecular evolution along different lineages in a phylogeny and link these rates with observations in extant species, such as convergent phenotypes. Pipelines for such work can help identify when and where genomic changes may be associated with, or possibly influence, phenotypic traits. We recently developed a set of models called PhyloAcc, using a Bayesian framework to estimate rates of nucleotide substitution on different branches of a phylogenetic tree and evaluate their association with pre-defined or estimated phenotypic traits. PhyloAcc-ST and PhyloAcc-GT both allow users to define a priori a set of target lineages and then compare different models to identify loci accelerating in one or more target lineages. Whereas ST considers only one species tree across all input loci, GT considers alternate topologies for every locus. PhyloAcc-C simultaneously models molecular rates and rates of continuous trait evolution, allowing the user to ask whether the two are associated. Here, we describe these models and provide tips and workflows on how to prepare the input data and run PhyloAcc.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1513-1525"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579529/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141181588","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nigel K Anderson, Doris Preininger, Matthew J Fuxjager
To humans, the diverse array of display behaviors that animals use for communication can easily seem peculiar or bizarre. While ample research delves into the evolutionary principles that shape these signals' effectiveness, little attention is paid to evolutionary patterning of signal design across taxa, particularly when it comes to the potential convergent evolution of many elaborate behavioral displays. By taking a mechanistic perspective, we explore the physiological and neurobiological mechanisms that likely influence the evolution of communication signals, emphasizing the utilization of pre-existing structures over novel adaptations. Central to this investigation are the concepts of perceptual bias and ritualization that we propose contribute to the convergence of elaborate display designs across species. Perceptual bias explains a phenomenon where pre-existing perceptual systems of receivers, used for innate behaviors such as food and predator recognition, select for certain traits of a communication signal from a signaler. Ritualization occurs when traits with no functional role in communication are co-opted through selection and transformed into a new communicative signal. Importantly, susceptibility for ritualization can be brought about through physiological modifications that occurred early in evolutionary time. In this way, perceptual bias can be a selective force that causes the co-option of non-communicative traits into a new communication signal through ritualization involving pre-existing modifications to physiological systems. If the perceptual bias, non-communicative signal, and physiological modifications that increase susceptibility to ritualization are highly conserved, then we may see the convergent evolution of the new communication signal with unrelated taxa facing similar sensory constraints. We explore this idea here using the foot-flagging frog system as a theoretical case study.
{"title":"Physiological Basis of Convergent Evolution in Animal Communication Systems.","authors":"Nigel K Anderson, Doris Preininger, Matthew J Fuxjager","doi":"10.1093/icb/icae091","DOIUrl":"10.1093/icb/icae091","url":null,"abstract":"<p><p>To humans, the diverse array of display behaviors that animals use for communication can easily seem peculiar or bizarre. While ample research delves into the evolutionary principles that shape these signals' effectiveness, little attention is paid to evolutionary patterning of signal design across taxa, particularly when it comes to the potential convergent evolution of many elaborate behavioral displays. By taking a mechanistic perspective, we explore the physiological and neurobiological mechanisms that likely influence the evolution of communication signals, emphasizing the utilization of pre-existing structures over novel adaptations. Central to this investigation are the concepts of perceptual bias and ritualization that we propose contribute to the convergence of elaborate display designs across species. Perceptual bias explains a phenomenon where pre-existing perceptual systems of receivers, used for innate behaviors such as food and predator recognition, select for certain traits of a communication signal from a signaler. Ritualization occurs when traits with no functional role in communication are co-opted through selection and transformed into a new communicative signal. Importantly, susceptibility for ritualization can be brought about through physiological modifications that occurred early in evolutionary time. In this way, perceptual bias can be a selective force that causes the co-option of non-communicative traits into a new communication signal through ritualization involving pre-existing modifications to physiological systems. If the perceptual bias, non-communicative signal, and physiological modifications that increase susceptibility to ritualization are highly conserved, then we may see the convergent evolution of the new communication signal with unrelated taxa facing similar sensory constraints. We explore this idea here using the foot-flagging frog system as a theoretical case study.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1422-1436"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141472805","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Strong selective pressure on phenotype can arise when habitat transitions fundamentally alter the physical media in which animals live, such as the invasion of land by lobe-finned fishes and insects. When environmental gradients differ drastically among habitats and multiple lineages transition between these habitats, we expect phenotypic convergence to be prevalent. One transition where widespread convergence has been observed is the shift from aboveground to subterranean environments in fossorial animals. Subterranean environments are low-light, confined spaces and tend to be hypoxic or anoxic, not to mention that the act of burrowing itself demands morphological specializations for excavation. Research suggests burrowing promotes morphological convergence in crayfish, with non-burrowing forms having a dorsoventrally compressed carapace and long, slender claws (chelae), while primary burrowing forms have a dorsolaterally compressed carapace and shorter, more powerful claws. However, earlier ecomorphological comparisons relied on qualitative rather than quantitative assessments of phenotypic differences. This study tested for convergence in North American crayfishes using a geometric morphometric approach. We photographed the carapace and claw for representative species across 13 North American genera. We hypothesized that crayfishes that occur in similar habitats and exhibit similar burrowing behaviors, would converge in their carapace and claw shapes. We found evidence for convergence in carapace and claw morphologies in burrowing crayfishes. However, claw phenotypes did not converge as strongly as carapace shape, an example of "imperfect" or "incomplete" convergence we attribute to the multiple competing demands on claw form and function. We argue that nuances in habitat characteristics, like soil type or compaction, make complete convergence unlikely for range- and dispersal-limited fossorial crayfishes.
{"title":"Burrowing Constrains the Phenotypic Diversity of Fossorial Crayfish.","authors":"Emmy M Delekta, Matthew A Kolmann","doi":"10.1093/icb/icae067","DOIUrl":"10.1093/icb/icae067","url":null,"abstract":"<p><p>Strong selective pressure on phenotype can arise when habitat transitions fundamentally alter the physical media in which animals live, such as the invasion of land by lobe-finned fishes and insects. When environmental gradients differ drastically among habitats and multiple lineages transition between these habitats, we expect phenotypic convergence to be prevalent. One transition where widespread convergence has been observed is the shift from aboveground to subterranean environments in fossorial animals. Subterranean environments are low-light, confined spaces and tend to be hypoxic or anoxic, not to mention that the act of burrowing itself demands morphological specializations for excavation. Research suggests burrowing promotes morphological convergence in crayfish, with non-burrowing forms having a dorsoventrally compressed carapace and long, slender claws (chelae), while primary burrowing forms have a dorsolaterally compressed carapace and shorter, more powerful claws. However, earlier ecomorphological comparisons relied on qualitative rather than quantitative assessments of phenotypic differences. This study tested for convergence in North American crayfishes using a geometric morphometric approach. We photographed the carapace and claw for representative species across 13 North American genera. We hypothesized that crayfishes that occur in similar habitats and exhibit similar burrowing behaviors, would converge in their carapace and claw shapes. We found evidence for convergence in carapace and claw morphologies in burrowing crayfishes. However, claw phenotypes did not converge as strongly as carapace shape, an example of \"imperfect\" or \"incomplete\" convergence we attribute to the multiple competing demands on claw form and function. We argue that nuances in habitat characteristics, like soil type or compaction, make complete convergence unlikely for range- and dispersal-limited fossorial crayfishes.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1454-1466"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141307466","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jennifer L Fenner, Callum Newberry, Callie Todd, Ryan C Range
How animal body plans evolved and diversified is a major question in evolutionary developmental biology. To address this question, it is important to characterize the exact molecular mechanisms that establish the major embryonic axes that give rise to the adult animal body plan. The anterior-posterior (AP) axis is the first axis to be established in most animal embryos, and in echinoderm sea urchin embryos its formation is governed by an integrated network of three different Wnt signaling pathways: Wnt/β-catenin, Wnt/JNK, and Wnt/PKC pathways. The extent to which this embryonic patterning mechanism is conserved among deuterostomes, or more broadly in metazoans, is an important open question whose answers could lead to a deeper appreciation of the evolution of the AP axis. Because Ambulacrarians (echinoderms and hemichordates) reside in a key phylogenetic position as the sister group to chordates, studies in these animals can help inform on how chordate body plans may have evolved. Here, we assayed the spatiotemporal gene expression of a subset of sea urchin AP Wnt patterning gene orthologs in the hemichordate, Schizocardium californicum. Our results show that positioning of the anterior neuroectoderm (ANE) to a territory around the anterior pole during early AP formation is spatially and temporally similar between indirect developing hemichordates and sea urchins. Furthermore, we show that the expression of wnt8 and frizzled5/8, two known drivers of ANE patterning in sea urchins, is similar in hemichordate embryos. Lastly, our results highlight divergence in embryonic expression of several early expressed Wnt genes (wnt1, wnt2, and wnt4). These results suggest that expression of the sea urchin AP Wnt signaling network is largely conserved in indirect developing hemichordates setting the foundation for future functional studies in S. californicum.
动物身体结构是如何进化和多样化的,这是进化发育生物学的一个重要问题。要解决这个问题,就必须确定建立主要胚胎轴线的确切分子机制,这些轴线会产生成年动物的体型。前后轴(AP)是大多数动物胚胎中最先建立的轴,在棘皮动物海胆胚胎中,它的形成受三种不同 Wnt 信号通路的综合网络控制:在棘皮动物海胆胚胎中,它的形成受三种不同 Wnt 信号通路的综合网络控制:Wnt/β-catenin、Wnt/JNK 和 Wnt/PKC 通路。这种胚胎模式化机制在中胚层动物或更广泛的后生动物中的保守程度是一个重要的悬而未决的问题。由于伏棘动物(棘皮动物和半脊索动物)作为脊索动物的姊妹群处于系统发育的关键位置,对这些动物的研究有助于了解脊索动物的身体结构是如何进化的。在这里,我们检测了半脊索动物 Schizocardium californicum 中海胆 AP Wnt 模式基因直向同源物亚群的时空基因表达。我们的研究结果表明,在早期AP形成过程中,前神经外胚层(ANE)在前极周围的定位在空间和时间上与间接发育的半脊索动物和海胆相似。此外,我们还发现 wnt8 和 frizzled5/8 这两种已知的海胆 ANE 形态形成的驱动因子在半脊柱动物胚胎中的表达相似。最后,我们的研究结果突显了几个早期表达的 Wnt 基因(wnt1、wnt2 和 wnt4)在胚胎期表达的差异。这些结果表明,海胆 AP Wnt 信号网络的表达在间接发育的半脊柱动物中基本上是保守的,这为今后在 S. californicum 中进行功能研究奠定了基础。
{"title":"Anterior-Posterior Wnt Signaling Network Conservation between Indirect Developing Sea Urchin and Hemichordate Embryos.","authors":"Jennifer L Fenner, Callum Newberry, Callie Todd, Ryan C Range","doi":"10.1093/icb/icae047","DOIUrl":"10.1093/icb/icae047","url":null,"abstract":"<p><p>How animal body plans evolved and diversified is a major question in evolutionary developmental biology. To address this question, it is important to characterize the exact molecular mechanisms that establish the major embryonic axes that give rise to the adult animal body plan. The anterior-posterior (AP) axis is the first axis to be established in most animal embryos, and in echinoderm sea urchin embryos its formation is governed by an integrated network of three different Wnt signaling pathways: Wnt/β-catenin, Wnt/JNK, and Wnt/PKC pathways. The extent to which this embryonic patterning mechanism is conserved among deuterostomes, or more broadly in metazoans, is an important open question whose answers could lead to a deeper appreciation of the evolution of the AP axis. Because Ambulacrarians (echinoderms and hemichordates) reside in a key phylogenetic position as the sister group to chordates, studies in these animals can help inform on how chordate body plans may have evolved. Here, we assayed the spatiotemporal gene expression of a subset of sea urchin AP Wnt patterning gene orthologs in the hemichordate, Schizocardium californicum. Our results show that positioning of the anterior neuroectoderm (ANE) to a territory around the anterior pole during early AP formation is spatially and temporally similar between indirect developing hemichordates and sea urchins. Furthermore, we show that the expression of wnt8 and frizzled5/8, two known drivers of ANE patterning in sea urchins, is similar in hemichordate embryos. Lastly, our results highlight divergence in embryonic expression of several early expressed Wnt genes (wnt1, wnt2, and wnt4). These results suggest that expression of the sea urchin AP Wnt signaling network is largely conserved in indirect developing hemichordates setting the foundation for future functional studies in S. californicum.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1214-1225"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579615/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141071584","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}