Clayton J. Harry, Sonia M. Messar, Erik J. Ragsdale
Pristionchus pacificus is a nematode model for the developmental genetics of morphological polyphenism, especially at the level of individual cells. Morphological polyphenism in this species includes an evolutionary novelty, moveable teeth, which have enabled predatory feeding in this species and others in its family (Diplogastridae). From transmission electron micrographs of serial thin sections through an adult hermaphrodite of P. pacificus, we three-dimensionally reconstructed all epithelial and myoepithelial cells and syncytia, corresponding to 74 nuclei, of its face, mouth, and pharynx. We found that the epithelia that produce the predatory morphology of P. pacificus are identical to Caenorhabditis elegans in the number of cell classes and nuclei. However, differences in cell form, spatial relationships, and nucleus position correlate with gross morphological differences from C. elegans and outgroups. Moreover, we identified fine-structural features, especially in the anteriormost pharyngeal muscles, that underlie the conspicuous, left-right asymmetry that characterizes the P. pacificus feeding apparatus. Our reconstruction provides an anatomical map for studying the genetics of polyphenism, feeding behavior, and the development of novel form in a satellite model to C. elegans.
{"title":"Comparative reconstruction of the predatory feeding structures of the polyphenic nematode Pristionchus pacificus","authors":"Clayton J. Harry, Sonia M. Messar, Erik J. Ragsdale","doi":"10.1111/ede.12397","DOIUrl":"10.1111/ede.12397","url":null,"abstract":"<p><i>Pristionchus pacificus</i> is a nematode model for the developmental genetics of morphological polyphenism, especially at the level of individual cells. Morphological polyphenism in this species includes an evolutionary novelty, moveable teeth, which have enabled predatory feeding in this species and others in its family (Diplogastridae). From transmission electron micrographs of serial thin sections through an adult hermaphrodite of <i>P. pacificus</i>, we three-dimensionally reconstructed all epithelial and myoepithelial cells and syncytia, corresponding to 74 nuclei, of its face, mouth, and pharynx. We found that the epithelia that produce the predatory morphology of <i>P. pacificus</i> are identical to <i>Caenorhabditis elegans</i> in the number of cell classes and nuclei. However, differences in cell form, spatial relationships, and nucleus position correlate with gross morphological differences from <i>C. elegans</i> and outgroups. Moreover, we identified fine-structural features, especially in the anteriormost pharyngeal muscles, that underlie the conspicuous, left-right asymmetry that characterizes the <i>P. pacificus</i> feeding apparatus. Our reconstruction provides an anatomical map for studying the genetics of polyphenism, feeding behavior, and the development of novel form in a satellite model to <i>C. elegans</i>.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"24 1-2","pages":"16-36"},"PeriodicalIF":2.9,"publicationDate":"2022-03-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12397","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"46116949","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}
The evolution of gene expression via cis-regulatory changes is well established as a major driver of phenotypic evolution. However, relatively little is known about the influence of enhancer architecture and intergenic interactions on regulatory evolution. We address this question by examining chemosensory system evolution in Drosophila. Drosophila prolongata males show a massively increased number of chemosensory bristles compared to females and males of sibling species. This increase is driven by sex-specific transformation of ancestrally mechanosensory organs. Consistent with this phenotype, the Pox neuro transcription factor (Poxn), which specifies chemosensory bristle identity, shows expanded expression in D. prolongata males. Poxn expression is controlled by nonadditive interactions among widely dispersed enhancers. Although some D. prolongata Poxn enhancers show increased activity, the additive component of this increase is slight, suggesting that most changes in Poxn expression are due to epistatic interactions between Poxn enhancers and trans-regulatory factors. Indeed, the expansion of D. prolongata Poxn enhancer activity is only observed in cells that express doublesex (dsx), the gene that controls sexual differentiation in Drosophila and also shows increased expression in D. prolongata males due to cis-regulatory changes. Although expanded dsx expression may contribute to increased activity of D. prolongata Poxn enhancers, this interaction is not sufficient to explain the full expansion of Poxn expression, suggesting that cis–trans interactions between Poxn, dsx, and additional unknown genes are necessary to produce the derived D. prolongata phenotype. Overall, our results demonstrate the importance of epistatic gene interactions for evolution, particularly when pivotal genes have complex regulatory architecture.
{"title":"Sex-specific evolution of a Drosophila sensory system via interacting cis- and trans-regulatory changes","authors":"David Luecke, Gavin Rice, Artyom Kopp","doi":"10.1111/ede.12398","DOIUrl":"10.1111/ede.12398","url":null,"abstract":"<p>The evolution of gene expression via <i>cis</i>-regulatory changes is well established as a major driver of phenotypic evolution. However, relatively little is known about the influence of enhancer architecture and intergenic interactions on regulatory evolution. We address this question by examining chemosensory system evolution in <i>Drosophila</i>. <i>Drosophila prolongata</i> males show a massively increased number of chemosensory bristles compared to females and males of sibling species. This increase is driven by sex-specific transformation of ancestrally mechanosensory organs. Consistent with this phenotype, the <i>Pox neuro</i> transcription factor (<i>Poxn</i>), which specifies chemosensory bristle identity, shows expanded expression in <i>D. prolongata</i> males. <i>Poxn</i> expression is controlled by nonadditive interactions among widely dispersed enhancers. Although some <i>D. prolongata Poxn</i> enhancers show increased activity, the additive component of this increase is slight, suggesting that most changes in <i>Poxn</i> expression are due to epistatic interactions between <i>Poxn</i> enhancers and <i>trans</i>-regulatory factors. Indeed, the expansion of <i>D. prolongata Poxn</i> enhancer activity is only observed in cells that express <i>doublesex</i> (<i>dsx</i>), the gene that controls sexual differentiation in <i>Drosophila</i> and also shows increased expression in <i>D. prolongata</i> males due to <i>cis</i>-regulatory changes. Although expanded <i>dsx</i> expression may contribute to increased activity of <i>D. prolongata Poxn</i> enhancers, this interaction is not sufficient to explain the full expansion of <i>Poxn</i> expression, suggesting that <i>cis</i>–<i>trans</i> interactions between <i>Poxn, dsx</i>, and additional unknown genes are necessary to produce the derived <i>D. prolongata</i> phenotype. Overall, our results demonstrate the importance of epistatic gene interactions for evolution, particularly when pivotal genes have complex regulatory architecture.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"24 1-2","pages":"37-60"},"PeriodicalIF":2.9,"publicationDate":"2022-03-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9075528","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}
Richard J. Walters, David Berger, Wolf U. Blanckenhorn, Luc F. Bussière, Patrick T. Rohner, Ralf Jochmann, Karin Thüler, Martin A. Schäfer
Understanding how environmental variation influences even cryptic traits is important to clarify the roles of selection and developmental constraints in past evolutionary divergence and to predict future adaptation under environmental change. Female yellow dung flies (Scathophaga stercoraria) typically have three sperm storage compartments (3S), but occasionally four (4S). More spermathecae are thought to be a female adaptation facilitating sperm sorting after mating, but the phenotype is very rare in nature. We manipulated the flies' developmental environment by food restriction, pesticides, and hot temperatures to investigate the nature and extent of developmental plasticity of this trait, and whether spermatheca expression correlates with measures of performance and developmental stability, as would be expected if 4S expression is a developmental aberration. The spermathecal polymorphism of yellow dung fly females is heritable, but also highly developmentally plastic, varying strongly with rearing conditions. 4S expression is tightly linked to growth rate, and weakly positively correlated with fluctuating asymmetry of wings and legs, suggesting that the production of a fourth spermatheca could be a nonadaptive developmental aberration. However, spermathecal plasticity is opposite in the closely related and ecologically similar Scathophaga suilla, demonstrating that overexpression of spermathecae under developmental stress is not universal. At the same time, we found overall mortality costs as well as benefits of 4S pheno- and genotypes (also affecting male siblings), suggesting that a life history trade-off may potentially moderate 4S expression. We conclude that the release of cryptic genetic variation in spermatheca number in the face of strong environmental variation may expose hidden traits (here reproductive morphology) to natural selection (here under climate warming or food augmentation). Once exposed, hidden traits can potentially undergo rapid genetic assimilation, even in cases when trait changes are first triggered by random errors that destabilize developmental processes.
{"title":"Growth rate mediates hidden developmental plasticity of female yellow dung fly reproductive morphology in response to environmental stressors","authors":"Richard J. Walters, David Berger, Wolf U. Blanckenhorn, Luc F. Bussière, Patrick T. Rohner, Ralf Jochmann, Karin Thüler, Martin A. Schäfer","doi":"10.1111/ede.12396","DOIUrl":"10.1111/ede.12396","url":null,"abstract":"<p>Understanding how environmental variation influences even cryptic traits is important to clarify the roles of selection and developmental constraints in past evolutionary divergence and to predict future adaptation under environmental change. Female yellow dung flies (<i>Scathophaga stercoraria</i>) typically have three sperm storage compartments (3S), but occasionally four (4S). More spermathecae are thought to be a female adaptation facilitating sperm sorting after mating, but the phenotype is very rare in nature. We manipulated the flies' developmental environment by food restriction, pesticides, and hot temperatures to investigate the nature and extent of developmental plasticity of this trait, and whether spermatheca expression correlates with measures of performance and developmental stability, as would be expected if 4S expression is a developmental aberration. The spermathecal polymorphism of yellow dung fly females is heritable, but also highly developmentally plastic, varying strongly with rearing conditions. 4S expression is tightly linked to growth rate, and weakly positively correlated with fluctuating asymmetry of wings and legs, suggesting that the production of a fourth spermatheca could be a nonadaptive developmental aberration. However, spermathecal plasticity is opposite in the closely related and ecologically similar <i>Scathophaga suilla</i>, demonstrating that overexpression of spermathecae under developmental stress is not universal. At the same time, we found overall mortality costs as well as benefits of 4S pheno- and genotypes (also affecting male siblings), suggesting that a life history trade-off may potentially moderate 4S expression. We conclude that the release of cryptic genetic variation in spermatheca number in the face of strong environmental variation may expose hidden traits (here reproductive morphology) to natural selection (here under climate warming or food augmentation). Once exposed, hidden traits can potentially undergo rapid genetic assimilation, even in cases when trait changes are first triggered by random errors that destabilize developmental processes.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"24 1-2","pages":"3-15"},"PeriodicalIF":2.9,"publicationDate":"2022-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9285807/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39731644","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}
Elena F. Boer, Emily T. Maclary, Michael D. Shapiro
Deciphering the genetic basis of vertebrate craniofacial variation is a longstanding biological problem with broad implications in evolution, development, and human pathology. One of the most stunning examples of craniofacial diversification is the adaptive radiation of birds, in which the beak serves essential roles in virtually every aspect of their life histories. The domestic pigeon (Columba livia) provides an exceptional opportunity to study the genetic underpinnings of craniofacial variation because of its unique balance of experimental accessibility and extraordinary phenotypic diversity within a single species. We used traditional and geometric morphometrics to quantify craniofacial variation in an F2 laboratory cross derived from the straight-beaked Pomeranian Pouter and curved-beak Scandaroon pigeon breeds. Using a combination of genome-wide quantitative trait locus scans and multi-locus modeling, we identified a set of genetic loci associated with complex shape variation in the craniofacial skeleton, including beak shape, braincase shape, and mandible shape. Some of these loci control coordinated changes between different structures, while others explain variation in the size and shape of specific skull and jaw regions. We find that in domestic pigeons, a complex blend of both independent and coupled genetic effects underlie three-dimensional craniofacial morphology.
{"title":"Complex genetic architecture of three-dimensional craniofacial shape variation in domestic pigeons","authors":"Elena F. Boer, Emily T. Maclary, Michael D. Shapiro","doi":"10.1111/ede.12395","DOIUrl":"10.1111/ede.12395","url":null,"abstract":"<p>Deciphering the genetic basis of vertebrate craniofacial variation is a longstanding biological problem with broad implications in evolution, development, and human pathology. One of the most stunning examples of craniofacial diversification is the adaptive radiation of birds, in which the beak serves essential roles in virtually every aspect of their life histories. The domestic pigeon (<i>Columba livia</i>) provides an exceptional opportunity to study the genetic underpinnings of craniofacial variation because of its unique balance of experimental accessibility and extraordinary phenotypic diversity within a single species. We used traditional and geometric morphometrics to quantify craniofacial variation in an F<sub>2</sub> laboratory cross derived from the straight-beaked Pomeranian Pouter and curved-beak Scandaroon pigeon breeds. Using a combination of genome-wide quantitative trait locus scans and multi-locus modeling, we identified a set of genetic loci associated with complex shape variation in the craniofacial skeleton, including beak shape, braincase shape, and mandible shape. Some of these loci control coordinated changes between different structures, while others explain variation in the size and shape of specific skull and jaw regions. We find that in domestic pigeons, a complex blend of both independent and coupled genetic effects underlie three-dimensional craniofacial morphology.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"23 6","pages":"477-495"},"PeriodicalIF":2.9,"publicationDate":"2021-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/0c/80/EDE-23-477.PMC9119316.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39607941","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}
Extant and fossil pterobranchs show distinct symmetry conditions of the individual zooids and their tubaria that are not necessarily comparable. The strict bilateral symmetry in the zooids of extant Cephalodiscida is modified to a considerable anatomical asymmetry in extant Rhabdopleurida. This type of left–right asymmetry can be recognized as antisymmetry, as dextral and sinistral developments are equally common. Antisymmetry is also recognized in the rhabdopleurid tubaria and in the proximal development and branching of planktic graptoloids. The antisymmetry of the graptoloid tubarium is modified during the Tremadocian time interval to a fixed or directional asymmetry. From the latest Tremadocian or earliest Floian onwards, proximal development in the Graptoloidea is invariably dextral and very few examples of a sinistral development have been found. The transition from antisymmetry to directional asymmetry can only be recognized in the graptolite tubaria, as the anatomy of the zooids is unknown from the fossil record. Directional asymmetry is not recognized in extant Pterobranchia.
{"title":"Symmetry in graptolite zooids and tubaria (Pterobranchia, Hemichordata)","authors":"Jörg Maletz","doi":"10.1111/ede.12394","DOIUrl":"10.1111/ede.12394","url":null,"abstract":"<p>Extant and fossil pterobranchs show distinct symmetry conditions of the individual zooids and their tubaria that are not necessarily comparable. The strict bilateral symmetry in the zooids of extant Cephalodiscida is modified to a considerable anatomical asymmetry in extant Rhabdopleurida. This type of left–right asymmetry can be recognized as antisymmetry, as dextral and sinistral developments are equally common. Antisymmetry is also recognized in the rhabdopleurid tubaria and in the proximal development and branching of planktic graptoloids. The antisymmetry of the graptoloid tubarium is modified during the Tremadocian time interval to a fixed or directional asymmetry. From the latest Tremadocian or earliest Floian onwards, proximal development in the Graptoloidea is invariably dextral and very few examples of a sinistral development have been found. The transition from antisymmetry to directional asymmetry can only be recognized in the graptolite tubaria, as the anatomy of the zooids is unknown from the fossil record. Directional asymmetry is not recognized in extant Pterobranchia.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"23 6","pages":"513-523"},"PeriodicalIF":2.9,"publicationDate":"2021-12-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12394","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39723438","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}
Jillian D. Oliver, Katrina E. Jones, Stephanie E. Pierce, Lionel Hautier
Xenarthrans (armadillos, anteaters, sloths, and their extinct relatives) are unique among mammals in displaying a distinctive specialization of the posterior trunk vertebrae—supernumerary vertebral xenarthrous articulations. This study seeks to understand how xenarthry develops through ontogeny and if it may be constrained to appear within pre-existing vertebral regions. Using three-dimensional geometric morphometrics on the neural arches of vertebrae, we explore phenotypic, allometric, and disparity patterns of the different axial morphotypes during the ontogeny of nine-banded armadillos. Shape-based regionalization analyses showed that the adult thoracolumbar column is divided into three regions according to the presence or absence of ribs and the presence or absence of xenarthrous articulations. A three-region division was retrieved in almost all specimens through development, although younger stages (e.g., fetuses, neonates) have more region boundary variability. In size-based regionalization analyses, thoracolumbar vertebrae are separated into two regions: a prediaphragmatic, prexenarthrous region, and a postdiaphragmatic xenarthrous region. We show that posterior thoracic vertebrae grow at a slower rate, while anterior thoracics and lumbars grow at a faster rate relatively, with rates decreasing anteroposteriorly in the former and increasing anteroposteriorly in the latter. We propose that different proportions between vertebrae and vertebral regions might result from differences in growth pattern and timing of ossification.
{"title":"Size and shape regional differentiation during the development of the spine in the nine-banded armadillo (Dasypus novemcinctus)","authors":"Jillian D. Oliver, Katrina E. Jones, Stephanie E. Pierce, Lionel Hautier","doi":"10.1111/ede.12393","DOIUrl":"10.1111/ede.12393","url":null,"abstract":"<p>Xenarthrans (armadillos, anteaters, sloths, and their extinct relatives) are unique among mammals in displaying a distinctive specialization of the posterior trunk vertebrae—supernumerary vertebral xenarthrous articulations. This study seeks to understand how xenarthry develops through ontogeny and if it may be constrained to appear within pre-existing vertebral regions. Using three-dimensional geometric morphometrics on the neural arches of vertebrae, we explore phenotypic, allometric, and disparity patterns of the different axial morphotypes during the ontogeny of nine-banded armadillos. Shape-based regionalization analyses showed that the adult thoracolumbar column is divided into three regions according to the presence or absence of ribs and the presence or absence of xenarthrous articulations. A three-region division was retrieved in almost all specimens through development, although younger stages (e.g., fetuses, neonates) have more region boundary variability. In size-based regionalization analyses, thoracolumbar vertebrae are separated into two regions: a prediaphragmatic, prexenarthrous region, and a postdiaphragmatic xenarthrous region. We show that posterior thoracic vertebrae grow at a slower rate, while anterior thoracics and lumbars grow at a faster rate relatively, with rates decreasing anteroposteriorly in the former and increasing anteroposteriorly in the latter. We propose that different proportions between vertebrae and vertebral regions might result from differences in growth pattern and timing of ossification.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"23 6","pages":"496-512"},"PeriodicalIF":2.9,"publicationDate":"2021-11-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39904008","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}