Kathryn Wilsterman, Anna Isabel Bautista, Chloe E Butler, Makenna Y Juergens, Ashley M Larson
Relative reproductive success and failure are the ultimate determinants of Darwinian fitness. As such, reproductive traits and variations therein have an immediate and considerable impact on the evolutionary trajectory of lineages. Historically, significant attention has been paid to the ecological and evolutionary processes (ultimate factors) that shape the diversity and canalization of reproductive traits within groups to better our understanding of organismal diversity and population or species resilience. In contrast, the physiological systems that mediate variation within and among species (i.e., the proximate factors) in reproductive traits remain a significant black box. To date, there is comparatively little information about how proximate mechanisms constrain or promote evolutionary potential in reproductive traits. In this mini-review, we focus on litter size in Eutherian mammals as a trait with relatively well-defined diversity (litter sizes are well-described both within and across species) and for which some genetic determinants have been identified. We discuss both the ultimate and potential proximate determinants of litter size with special attention to the breadth of physiological traits that may act as "toggle" switches for evolution of litter size. We close with a brief discussion of the role that physiological plasticity may play in the evolution of litter size and lay out several forward-looking areas for future research.
{"title":"Evolution of Litter Size: Proximate and Ultimate Mechanisms.","authors":"Kathryn Wilsterman, Anna Isabel Bautista, Chloe E Butler, Makenna Y Juergens, Ashley M Larson","doi":"10.1093/icb/icae052","DOIUrl":"10.1093/icb/icae052","url":null,"abstract":"<p><p>Relative reproductive success and failure are the ultimate determinants of Darwinian fitness. As such, reproductive traits and variations therein have an immediate and considerable impact on the evolutionary trajectory of lineages. Historically, significant attention has been paid to the ecological and evolutionary processes (ultimate factors) that shape the diversity and canalization of reproductive traits within groups to better our understanding of organismal diversity and population or species resilience. In contrast, the physiological systems that mediate variation within and among species (i.e., the proximate factors) in reproductive traits remain a significant black box. To date, there is comparatively little information about how proximate mechanisms constrain or promote evolutionary potential in reproductive traits. In this mini-review, we focus on litter size in Eutherian mammals as a trait with relatively well-defined diversity (litter sizes are well-described both within and across species) and for which some genetic determinants have been identified. We discuss both the ultimate and potential proximate determinants of litter size with special attention to the breadth of physiological traits that may act as \"toggle\" switches for evolution of litter size. We close with a brief discussion of the role that physiological plasticity may play in the evolution of litter size and lay out several forward-looking areas for future research.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1643-1660"},"PeriodicalIF":2.2,"publicationDate":"2024-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11659681/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141157635","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}
Basic science research, also called "curiosity-driven research," is fundamental work done with no immediate economic goals but rather a focus on discovery for discovery's sake. However, basic science research is often needed to seed more applied, economically-oriented, research. Both basic and applied research efforts are important aspects of the "bioeconomy" defined here as the contributions to the overall economy from various biology-related fields spanning everything from museum-based natural history research to agricultural food and material production to healthcare. Here we propose that more collaborative efforts across federal granting agencies in a venture-capitalist-like "PO-driven model" can help drive applied innovation from collaborations facilitated by Program Officers (PO). Program Officers from NSF, DOE, DARPA, USDA, NASA, and other federal agencies should seek out parallel and complementary research ideas from grantees and provide funds to build teams of researchers who may otherwise be unaware of one another. Researchers working in different field may also be unaware that the different organisms they are studying independently may have evolved similar traits (i.e., convergent evolution) that POs may recognize and who can then facilitate novel research avenues connecting those independent researchers (we provide examples of some projects inspired by convergent evolution here). In this top-down approach to research funding the U.S. bioeconomy will be pouring fuel on the fire of scientific productivity in this country.
{"title":"\"The PO-Driven Model\": A Basic Science Pipeline for the Bioeconomy with Solutions Inspired by Convergent Evolution for Connecting Parallel Research Ideas.","authors":"Tilottama Roy, Jung-Youn Lee, Tomokazu Kawashima, Grey Monroe, Prosanta Chakrabarty","doi":"10.1093/icb/icae156","DOIUrl":"https://doi.org/10.1093/icb/icae156","url":null,"abstract":"<p><p>Basic science research, also called \"curiosity-driven research,\" is fundamental work done with no immediate economic goals but rather a focus on discovery for discovery's sake. However, basic science research is often needed to seed more applied, economically-oriented, research. Both basic and applied research efforts are important aspects of the \"bioeconomy\" defined here as the contributions to the overall economy from various biology-related fields spanning everything from museum-based natural history research to agricultural food and material production to healthcare. Here we propose that more collaborative efforts across federal granting agencies in a venture-capitalist-like \"PO-driven model\" can help drive applied innovation from collaborations facilitated by Program Officers (PO). Program Officers from NSF, DOE, DARPA, USDA, NASA, and other federal agencies should seek out parallel and complementary research ideas from grantees and provide funds to build teams of researchers who may otherwise be unaware of one another. Researchers working in different field may also be unaware that the different organisms they are studying independently may have evolved similar traits (i.e., convergent evolution) that POs may recognize and who can then facilitate novel research avenues connecting those independent researchers (we provide examples of some projects inspired by convergent evolution here). In this top-down approach to research funding the U.S. bioeconomy will be pouring fuel on the fire of scientific productivity in this country.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142866487","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}
Kevin H Wong, Natalia Andrade Rodriguez, Nikki Traylor-Knowles
Single-cell RNA sequencing (scRNAseq) is a powerful tool to describe cell types in multicellular organisms across the animal kingdom. In standard scRNAseq analysis pipelines, clusters of cells with similar transcriptional signatures are given cell type labels based on marker genes that infer specialized known characteristics. Since these analyses are designed for model organisms, such as humans and mice, problems arise when attempting to label cell types of distantly related, non-model species that have unique or divergent cell types. Consequently, this leads to limited discovery of novel species-specific cell types and potential mis-annotation of cell types in non-model species while using scRNAseq. To address this problem, we discuss recently published approaches that help annotate scRNAseq clusters for any non-model organism. We first suggest that annotating with an evolutionary context of cell lineages will aid in the discovery of novel cell types and provide a marker-free approach to compare cell types across distantly related species. Secondly, machine learning has greatly improved bioinformatic analyses, so we highlight some open-source programs that use reference-free approaches to annotate cell clusters. Lastly, we propose the use of unannotated genes as potential cell markers for non-model organisms, as many do not have fully annotated genomes and these data are often disregarded. Improving single-cell annotations will aid the discovery of novel cell types and enhance our understanding of non-model organisms at a cellular level. By unifying approaches to annotate cell types in non-model organisms, we can increase the confidence of cell annotation label transfer and the flexibility to discover novel cell types.
{"title":"Exploring the Unknown: How Can We Improve Single-cell RNAseq Cell Type Annotations in Non-model Organisms?","authors":"Kevin H Wong, Natalia Andrade Rodriguez, Nikki Traylor-Knowles","doi":"10.1093/icb/icae112","DOIUrl":"10.1093/icb/icae112","url":null,"abstract":"<p><p>Single-cell RNA sequencing (scRNAseq) is a powerful tool to describe cell types in multicellular organisms across the animal kingdom. In standard scRNAseq analysis pipelines, clusters of cells with similar transcriptional signatures are given cell type labels based on marker genes that infer specialized known characteristics. Since these analyses are designed for model organisms, such as humans and mice, problems arise when attempting to label cell types of distantly related, non-model species that have unique or divergent cell types. Consequently, this leads to limited discovery of novel species-specific cell types and potential mis-annotation of cell types in non-model species while using scRNAseq. To address this problem, we discuss recently published approaches that help annotate scRNAseq clusters for any non-model organism. We first suggest that annotating with an evolutionary context of cell lineages will aid in the discovery of novel cell types and provide a marker-free approach to compare cell types across distantly related species. Secondly, machine learning has greatly improved bioinformatic analyses, so we highlight some open-source programs that use reference-free approaches to annotate cell clusters. Lastly, we propose the use of unannotated genes as potential cell markers for non-model organisms, as many do not have fully annotated genomes and these data are often disregarded. Improving single-cell annotations will aid the discovery of novel cell types and enhance our understanding of non-model organisms at a cellular level. By unifying approaches to annotate cell types in non-model organisms, we can increase the confidence of cell annotation label transfer and the flexibility to discover novel cell types.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1291-1299"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141629321","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}
M A Kolmann, E Poulin, J Rosen, D Hemraj-Naraine, M D Burns
Constraints on phenotypic evolution can lead to patterns of convergent evolution, by limiting the "pool" of potential phenotypes in the face of endogenous (functional, developmental) or exogenous (competition, predation) selective pressures. Evaluation of convergence depends on integrating ecological and morphological data within a robust, comparative phylogenetic context. The staggering diversity of teleost fishes offers a multitude of lineages adapted for similar ecological roles and, therefore, offers numerous replicated evolutionary experiments for exploring phenotypic convergence. However, our understanding of fish feeding systems has been primarily shaped by marine species, with the monolithic exception of freshwater cichlids. Here we use piranhas and pacus (Serrasalmidae) to explore the evolution of different feeding ecologies and their morphological proxies in Neotropical freshwater environments. Specifically, we explore whether convergence is more widespread among plant-eating fishes, arising from strong constraints on phenotypic evolution in herbivores. Using osteological micro-computed tomographic imaging (μCT), we describe the major axes of morphological variation in pacus and piranhas, regarding their diet and feeding behaviors. Next, we evaluated whether herbivorous niches are less labile than other dietary guilds and whether herbivorous species' phenotypes evolve at a slower evolutionary rate than other taxa. We then assess how convergent herbivorous taxa are, using three different suites of morphological characters (dental, jaw, and abdominal morphometrics). Ecologically, herbivory is not a dead end, exhibiting similar observed transition rates as those between carnivores and omnivores. However, we documented widespread convergence in herbivores and that herbivores have slower rates of phenotypic evolution than carnivores. Most instances of convergence are found in herbivorous taxa, specifically in frugivores and folivores. Moreover, instances of "complete" convergence, indicated by positive convergence metrics observed in more than one morphometric dataset, were only found in herbivores. Herbivores do appear to evolve under constrained circumstances, but this has not limited their ecological ability.
{"title":"Phenotypic Convergence Is Stronger and More Frequent in Herbivorous Fishes.","authors":"M A Kolmann, E Poulin, J Rosen, D Hemraj-Naraine, M D Burns","doi":"10.1093/icb/icae037","DOIUrl":"10.1093/icb/icae037","url":null,"abstract":"<p><p>Constraints on phenotypic evolution can lead to patterns of convergent evolution, by limiting the \"pool\" of potential phenotypes in the face of endogenous (functional, developmental) or exogenous (competition, predation) selective pressures. Evaluation of convergence depends on integrating ecological and morphological data within a robust, comparative phylogenetic context. The staggering diversity of teleost fishes offers a multitude of lineages adapted for similar ecological roles and, therefore, offers numerous replicated evolutionary experiments for exploring phenotypic convergence. However, our understanding of fish feeding systems has been primarily shaped by marine species, with the monolithic exception of freshwater cichlids. Here we use piranhas and pacus (Serrasalmidae) to explore the evolution of different feeding ecologies and their morphological proxies in Neotropical freshwater environments. Specifically, we explore whether convergence is more widespread among plant-eating fishes, arising from strong constraints on phenotypic evolution in herbivores. Using osteological micro-computed tomographic imaging (μCT), we describe the major axes of morphological variation in pacus and piranhas, regarding their diet and feeding behaviors. Next, we evaluated whether herbivorous niches are less labile than other dietary guilds and whether herbivorous species' phenotypes evolve at a slower evolutionary rate than other taxa. We then assess how convergent herbivorous taxa are, using three different suites of morphological characters (dental, jaw, and abdominal morphometrics). Ecologically, herbivory is not a dead end, exhibiting similar observed transition rates as those between carnivores and omnivores. However, we documented widespread convergence in herbivores and that herbivores have slower rates of phenotypic evolution than carnivores. Most instances of convergence are found in herbivorous taxa, specifically in frugivores and folivores. Moreover, instances of \"complete\" convergence, indicated by positive convergence metrics observed in more than one morphometric dataset, were only found in herbivores. Herbivores do appear to evolve under constrained circumstances, but this has not limited their ecological ability.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1467-1483"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140900401","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}
Alyssa M Hernandez, Perrin E Schiebel, Jennifer Shum, Robert J Wood
To navigate complex terrains, insects use diverse tarsal structures (adhesive pads, claws, spines) to reliably attach to and locomote across substrates. This includes surfaces of variable roughness and inclination, which often require reliable transitions from ambulatory to scansorial locomotion. Using bioinspired physical models as a means for comparative research, our study specifically focused on the diversity of tarsal spines, which facilitate locomotion via frictional engagement and shear force generation. For spine designs, we took inspiration from ground beetles (family: Carabidae), which is a largely terrestrial group known for their quick locomotion. Evaluating four different species, we found that the hind legs host linear rows of rigid spines along the entire tarsus. By taking morphometric measurements of the spines, we highlighted parameters of interest (e.g., spine angle and aspect ratio) in order to test their relationship to shear forces sustained during terrain interactions. We systematically evaluated these parameters using spines cut from stainless steel shim attached to a small acrylic sled loaded with various weights. The sled was placed on 3D-printed models of rough terrain, randomly generated using fractal Brownian motion, while a motorized pulley system applied force to the spines. A force sensor measured the reaction force on the terrain, recording shear force before failure occurred. Initial shear tests highlighted the importance of spine angle, with bioinspired anisotropic designs producing higher shear forces. Using these data, we placed the best (50° angle) and worst (90° angle) performing spines on the legs of our insect-scale ambulatory robot physical model. We then tested the robot on various surfaces at 0°, 10°, and 20° inclines, seeing similar success with the more bioinspired spines.
为了在复杂的地形上航行,昆虫利用各种跗关节结构(粘垫、爪、刺)可靠地附着在基质上并在基质上运动。这包括粗糙度和倾斜度各异的表面,而这些表面通常需要可靠地从伏地运动过渡到扫描运动。利用生物启发物理模型作为比较研究的手段,我们的研究特别关注跗骨棘的多样性,它通过摩擦啮合和产生剪切力来促进运动。在刺的设计方面,我们从地甲虫(甲壳虫科)中汲取了灵感,地甲虫主要是以快速运动著称的陆生类群。在对四个不同物种进行评估后,我们发现它们的后腿在整个跗节上都有一排线性的硬刺。通过对棘刺的形态测量,我们突出了感兴趣的参数(如棘刺角度和长宽比),以检验它们与地形相互作用时所承受的剪切力之间的关系。我们使用从不锈钢垫片上切割下来的脊柱系统地评估了这些参数,这些垫片连接在一个装有不同重量的小型丙烯酸雪橇上。雪橇被放置在利用分形布朗运动随机生成的粗糙地形 3D 打印模型上,同时电动滑轮系统对棘刺施力。力传感器测量地形上的反作用力,记录发生故障前的剪切力。最初的剪切测试强调了脊柱角度的重要性,生物启发各向异性设计产生的剪切力更大。利用这些数据,我们将性能最好(50°)和最差(90°)的脊柱放置在昆虫尺度可移动机器人物理模型的腿上。然后,我们在倾斜度为 0、10 和 20 ○ 的各种表面上对机器人进行了测试,结果显示,生物启发较多的棘刺取得了类似的成功。
{"title":"Spines and Inclines: Bioinspired Spines on an Insect-Scale Robot Facilitate Locomotion on Rough and Inclined Terrain.","authors":"Alyssa M Hernandez, Perrin E Schiebel, Jennifer Shum, Robert J Wood","doi":"10.1093/icb/icae145","DOIUrl":"10.1093/icb/icae145","url":null,"abstract":"<p><p>To navigate complex terrains, insects use diverse tarsal structures (adhesive pads, claws, spines) to reliably attach to and locomote across substrates. This includes surfaces of variable roughness and inclination, which often require reliable transitions from ambulatory to scansorial locomotion. Using bioinspired physical models as a means for comparative research, our study specifically focused on the diversity of tarsal spines, which facilitate locomotion via frictional engagement and shear force generation. For spine designs, we took inspiration from ground beetles (family: Carabidae), which is a largely terrestrial group known for their quick locomotion. Evaluating four different species, we found that the hind legs host linear rows of rigid spines along the entire tarsus. By taking morphometric measurements of the spines, we highlighted parameters of interest (e.g., spine angle and aspect ratio) in order to test their relationship to shear forces sustained during terrain interactions. We systematically evaluated these parameters using spines cut from stainless steel shim attached to a small acrylic sled loaded with various weights. The sled was placed on 3D-printed models of rough terrain, randomly generated using fractal Brownian motion, while a motorized pulley system applied force to the spines. A force sensor measured the reaction force on the terrain, recording shear force before failure occurred. Initial shear tests highlighted the importance of spine angle, with bioinspired anisotropic designs producing higher shear forces. Using these data, we placed the best (50° angle) and worst (90° angle) performing spines on the legs of our insect-scale ambulatory robot physical model. We then tested the robot on various surfaces at 0°, 10°, and 20° inclines, seeing similar success with the more bioinspired spines.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1371-1389"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142019629","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}
Sydney Popsuj, Lindsey Cohen, Sydney Ward, Arabella Lewis, Sean Yoshida, R Antonio Herrera, Christina D Cota, Alberto Stolfi
The evolutionary origins of chordates and their diversification into the three major subphyla of tunicates, vertebrates, and cephalochordates pose myriad questions about the genetic and developmental mechanisms underlying this radiation. Studies in non-vertebrate chordates have refined our model of what the ancestral chordate may have looked like, and have revealed the pre-vertebrate origins of key cellular and developmental traits. Work in the major tunicate laboratory model Ciona has benefitted greatly from the emergence of CRISPR/Cas9 techniques for targeted gene disruption. Here we review some of the important findings made possible by CRISPR in Ciona, and present our latest protocols and recommended practices for plasmid-based, tissue-specific CRISPR/Cas9-mediated mutagenesis.
{"title":"CRISPR/Cas9 Protocols for Disrupting Gene Function in the Non-vertebrate Chordate Ciona.","authors":"Sydney Popsuj, Lindsey Cohen, Sydney Ward, Arabella Lewis, Sean Yoshida, R Antonio Herrera, Christina D Cota, Alberto Stolfi","doi":"10.1093/icb/icae108","DOIUrl":"10.1093/icb/icae108","url":null,"abstract":"<p><p>The evolutionary origins of chordates and their diversification into the three major subphyla of tunicates, vertebrates, and cephalochordates pose myriad questions about the genetic and developmental mechanisms underlying this radiation. Studies in non-vertebrate chordates have refined our model of what the ancestral chordate may have looked like, and have revealed the pre-vertebrate origins of key cellular and developmental traits. Work in the major tunicate laboratory model Ciona has benefitted greatly from the emergence of CRISPR/Cas9 techniques for targeted gene disruption. Here we review some of the important findings made possible by CRISPR in Ciona, and present our latest protocols and recommended practices for plasmid-based, tissue-specific CRISPR/Cas9-mediated mutagenesis.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1182-1193"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11579527/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565148","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}
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}
Aaron H Griffing, Tony Gamble, Ashmika Behere, Timothy E Higham, Greta M Keller, John Resener, Thomas J Sanger
Adhesive toe pads have evolved numerous times over lizard evolutionary history, most notably in geckos. Despite significant variation in adult toe pad morphology across independent origins of toe pads, early developmental patterns of toe pad morphogenesis are similar among distantly related species. In these distant phylogenetic comparisons, toe pad variation is achieved during the later stages of development. We aimed to understand how toe pad variation is generated among species sharing a single evolutionary origin of toe pads (house geckos-Hemidactylus). We investigated toe pad functional variation and developmental patterns in three species of Hemidactylus, ranging from highly scansorial (H. platyurus), to less scansorial (H. turcicus), to fully terrestrial (H. imbricatus). We found that H. platyurus generated significantly greater frictional adhesive force and exhibited much larger toe pad area relative to the other two species. Furthermore, differences in the offset of toe pad extension phase during embryonic development results in the variable morphologies seen in adults. Taken together, we demonstrate how morphological variation is generated in a complex structure during development and how that variation relates in important functional outcomes.
{"title":"Developmental Patterns Underlying Variation in Form and Function Exhibited by House Gecko Toe Pads.","authors":"Aaron H Griffing, Tony Gamble, Ashmika Behere, Timothy E Higham, Greta M Keller, John Resener, Thomas J Sanger","doi":"10.1093/icb/icae008","DOIUrl":"10.1093/icb/icae008","url":null,"abstract":"<p><p>Adhesive toe pads have evolved numerous times over lizard evolutionary history, most notably in geckos. Despite significant variation in adult toe pad morphology across independent origins of toe pads, early developmental patterns of toe pad morphogenesis are similar among distantly related species. In these distant phylogenetic comparisons, toe pad variation is achieved during the later stages of development. We aimed to understand how toe pad variation is generated among species sharing a single evolutionary origin of toe pads (house geckos-Hemidactylus). We investigated toe pad functional variation and developmental patterns in three species of Hemidactylus, ranging from highly scansorial (H. platyurus), to less scansorial (H. turcicus), to fully terrestrial (H. imbricatus). We found that H. platyurus generated significantly greater frictional adhesive force and exhibited much larger toe pad area relative to the other two species. Furthermore, differences in the offset of toe pad extension phase during embryonic development results in the variable morphologies seen in adults. Taken together, we demonstrate how morphological variation is generated in a complex structure during development and how that variation relates in important functional outcomes.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1494-1504"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140295412","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}
Isabella V Changsut, Erin M Borbee, Haley R Womack, Alicia Shickle, Koty H Sharp, Lauren E Fuess
Scleractinian corals, essential ecosystem engineers that form the base of coral reef ecosystems, have faced unprecedented mortality in recent decades due to climate change-related stressors, including disease outbreaks. Despite this emergent threat to corals, many questions still remain regarding mechanisms underlying observed variation in disease susceptibility. Recent data suggest at least some degree of variation in disease response may be linked to variability in the relationship between host corals and their algal photosymbionts (Family Symbiodiniaceae). Still, the nuances of connections between symbiosis and immunity in cnidarians, including scleractinian corals, remain poorly understood. Here, we leveraged an emergent model species, the facultatively symbiotic, temperate, scleractinian coral Astrangia poculata, to investigate associations between symbiont density and both constitutive and induced immunity. We used a combination of controlled immune challenges with heat-inactivated pathogens and transcriptomic analyses. Our results demonstrate that A. poculata mounts a robust initial response to pathogenic stimuli that is highly similar to responses documented in tropical corals. We document positive associations between symbiont density and both constitutive and induced immune responses, in agreement with recent preliminary studies in A. poculata. A suite of immune genes, including those coding for antioxidant peroxiredoxin biosynthesis, are positively associated with symbiont density in A. poculata under constitutive conditions. Furthermore, variation in symbiont density is associated with distinct patterns of immune response; low symbiont density corals induce preventative immune mechanisms, whereas high symbiont density corals mobilize energetic resources to fuel humoral immune responses. In summary, our study reveals the need for more nuanced study of symbiosis-immune interplay across diverse scleractinian corals, preferably including quantitative energy budget analysis for full disentanglement of these complex associations and their effects on host pathogen susceptibility.
硬骨鱼类珊瑚是构成珊瑚礁生态系统基础的重要生态系统工程师,近几十年来,由于与气候变化相关的压力因素(包括疾病爆发),硬骨鱼类珊瑚面临着前所未有的死亡。尽管珊瑚面临着这一新出现的威胁,但关于所观察到的疾病易感性差异的内在机制仍存在许多问题。最近的数据表明,至少在某种程度上,疾病反应的变化可能与宿主珊瑚及其藻类光合共生体(共生藻科)之间关系的变化有关。然而,人们对包括硬骨珊瑚在内的刺胞动物的共生与免疫之间的微妙联系仍然知之甚少。在这里,我们利用新出现的模式物种--兼性共生的温带硬骨珊瑚 Astrangia poculata--来研究共生体密度与组成免疫和诱导免疫之间的关系。我们结合使用热灭活病原体进行受控免疫挑战和转录组分析。我们的研究结果表明,A. poculata 能对病原体刺激做出强有力的初始反应,这与热带珊瑚的反应非常相似。我们记录了共生体密度与组成型和诱导型免疫反应之间的正相关关系,这与最近对 A. poculata 的初步研究结果一致。在组成型条件下,A. poculata 的一系列免疫基因(包括抗氧化过氧化还原蛋白生物合成的编码基因)与共生体密度呈正相关。此外,共生体密度的变化还与不同的免疫反应模式有关;共生体密度低的珊瑚会诱导预防性免疫机制,而共生体密度高的珊瑚则会调动能量资源来促进体液免疫反应。总之,我们的研究表明,有必要对不同硬骨鱼类珊瑚的共生-免疫相互作用进行更细致的研究,最好包括定量能量预算分析,以全面理清这些复杂的关联及其对病原体易感性的影响。
{"title":"Photosymbiont Density Is Correlated with Constitutive and Induced Immunity in the Facultatively Symbiotic Coral, Astrangia poculata.","authors":"Isabella V Changsut, Erin M Borbee, Haley R Womack, Alicia Shickle, Koty H Sharp, Lauren E Fuess","doi":"10.1093/icb/icae036","DOIUrl":"10.1093/icb/icae036","url":null,"abstract":"<p><p>Scleractinian corals, essential ecosystem engineers that form the base of coral reef ecosystems, have faced unprecedented mortality in recent decades due to climate change-related stressors, including disease outbreaks. Despite this emergent threat to corals, many questions still remain regarding mechanisms underlying observed variation in disease susceptibility. Recent data suggest at least some degree of variation in disease response may be linked to variability in the relationship between host corals and their algal photosymbionts (Family Symbiodiniaceae). Still, the nuances of connections between symbiosis and immunity in cnidarians, including scleractinian corals, remain poorly understood. Here, we leveraged an emergent model species, the facultatively symbiotic, temperate, scleractinian coral Astrangia poculata, to investigate associations between symbiont density and both constitutive and induced immunity. We used a combination of controlled immune challenges with heat-inactivated pathogens and transcriptomic analyses. Our results demonstrate that A. poculata mounts a robust initial response to pathogenic stimuli that is highly similar to responses documented in tropical corals. We document positive associations between symbiont density and both constitutive and induced immune responses, in agreement with recent preliminary studies in A. poculata. A suite of immune genes, including those coding for antioxidant peroxiredoxin biosynthesis, are positively associated with symbiont density in A. poculata under constitutive conditions. Furthermore, variation in symbiont density is associated with distinct patterns of immune response; low symbiont density corals induce preventative immune mechanisms, whereas high symbiont density corals mobilize energetic resources to fuel humoral immune responses. In summary, our study reveals the need for more nuanced study of symbiosis-immune interplay across diverse scleractinian corals, preferably including quantitative energy budget analysis for full disentanglement of these complex associations and their effects on host pathogen susceptibility.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":"1278-1290"},"PeriodicalIF":2.2,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141089394","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}
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}