Protein-based materials are considered versatile biomaterials, and their biodegradability is an advantage for sustainable development. Bagworm produces strong silk for use in unique situations throughout its life stages. Rigorous molecular analyses of Eumeta variegata suggested that the particular mechanical properties of its silk are due to the coexistence of poly-A and GA motifs. However, little molecular information on closely related species is available, and it is not understood how these properties were acquired evolutionarily or whether the motif combination is a conserved trait in other bagworms. Here, we performed a transcriptome analysis of two other bagworm species (Canephora pungelerii and Bambalina sp.) belonging to the family Psychidae to elucidate the relationship between the fibroin gene and silk properties. The obtained transcriptome assemblies and tensile tests indicated that the motif combination and silk properties were conserved among the bagworms. Furthermore, our analysis showed that C. pungelerii produces extraordinarily strong silk (breaking strength of 1.4 GPa) and indicated that the cause may be the C. pungelerii -specific balance of crystalline/amorphous regions in the H-fibroin repetitive domain. This particular H-fibroin architecture may have been evolutionarily acquired to produce strong thread to maintain bag stability during the relatively long development period of Canephora species relative to other bagworms.
{"title":"The balance of crystalline and amorphous regions in the fibroin structure underpins the tensile strength of bagworm silk.","authors":"Nobuaki Kono, Hiroyuki Nakamura, Ayaka Tateishi, Keiji Numata, Kazuharu Arakawa","doi":"10.1186/s40851-021-00179-7","DOIUrl":"https://doi.org/10.1186/s40851-021-00179-7","url":null,"abstract":"<p><p>Protein-based materials are considered versatile biomaterials, and their biodegradability is an advantage for sustainable development. Bagworm produces strong silk for use in unique situations throughout its life stages. Rigorous molecular analyses of Eumeta variegata suggested that the particular mechanical properties of its silk are due to the coexistence of poly-A and GA motifs. However, little molecular information on closely related species is available, and it is not understood how these properties were acquired evolutionarily or whether the motif combination is a conserved trait in other bagworms. Here, we performed a transcriptome analysis of two other bagworm species (Canephora pungelerii and Bambalina sp.) belonging to the family Psychidae to elucidate the relationship between the fibroin gene and silk properties. The obtained transcriptome assemblies and tensile tests indicated that the motif combination and silk properties were conserved among the bagworms. Furthermore, our analysis showed that C. pungelerii produces extraordinarily strong silk (breaking strength of 1.4 GPa) and indicated that the cause may be the C. pungelerii -specific balance of crystalline/amorphous regions in the H-fibroin repetitive domain. This particular H-fibroin architecture may have been evolutionarily acquired to produce strong thread to maintain bag stability during the relatively long development period of Canephora species relative to other bagworms.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"11"},"PeriodicalIF":2.7,"publicationDate":"2021-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00179-7","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39224018","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}
Pub Date : 2021-06-21DOI: 10.1186/s40851-021-00175-x
Yoshio Takei
Adaptation to a hypertonic marine environment is one of the major topics in animal physiology research. Marine teleosts lose water osmotically from the gills and compensate for this loss by drinking surrounding seawater and absorbing water from the intestine. This situation is in contrast to that in mammals, which experience a net osmotic loss of water after drinking seawater. Water absorption in fishes is made possible by (1) removal of monovalent ions (desalinization) by the esophagus, (2) removal of divalent ions as carbonate (Mg/CaCO3) precipitates promoted by HCO3- secretion, and (3) facilitation of NaCl and water absorption from diluted seawater by the intestine using a suite of unique transporters. As a result, 70-85% of ingested seawater is absorbed during its passage through the digestive tract. Thus, the digestive tract is an essential organ for marine teleost survival in the hypertonic seawater environment. The eel is a species that has been frequently used for osmoregulation research in laboratories worldwide. The eel possesses many advantages as an experimental animal for osmoregulation studies, one of which is its outstanding euryhalinity, which enables researchers to examine changes in the structure and function of the digestive tract after direct transfer from freshwater to seawater. In recent years, the molecular mechanisms of ion and water transport across epithelial cells (the transcellular route) and through tight junctions (the paracellular route) have been elucidated for the esophagus and intestine. Thanks to the rapid progress in analytical methods for genome databases on teleosts, including the eel, the molecular identities of transporters, channels, pumps and junctional proteins have been clarified at the isoform level. As 10 y have passed since the previous reviews on this subject, it seems relevant and timely to summarize recent progress in research on the molecular mechanisms of water and ion transport in the digestive tract in eels and to compare the mechanisms with those of other teleosts and mammals from comparative and evolutionary viewpoints. We also propose future directions for this research field to achieve integrative understanding of the role of the digestive tract in adaptation to seawater with regard to pathways/mechanisms including the paracellular route, divalent ion absorption, metabolon formation and cellular trafficking of transporters. Notably, some of these have already attracted practical attention in laboratories.
{"title":"The digestive tract as an essential organ for water acquisition in marine teleosts: lessons from euryhaline eels.","authors":"Yoshio Takei","doi":"10.1186/s40851-021-00175-x","DOIUrl":"https://doi.org/10.1186/s40851-021-00175-x","url":null,"abstract":"<p><p>Adaptation to a hypertonic marine environment is one of the major topics in animal physiology research. Marine teleosts lose water osmotically from the gills and compensate for this loss by drinking surrounding seawater and absorbing water from the intestine. This situation is in contrast to that in mammals, which experience a net osmotic loss of water after drinking seawater. Water absorption in fishes is made possible by (1) removal of monovalent ions (desalinization) by the esophagus, (2) removal of divalent ions as carbonate (Mg/CaCO<sub>3</sub>) precipitates promoted by HCO<sub>3</sub><sup>-</sup> secretion, and (3) facilitation of NaCl and water absorption from diluted seawater by the intestine using a suite of unique transporters. As a result, 70-85% of ingested seawater is absorbed during its passage through the digestive tract. Thus, the digestive tract is an essential organ for marine teleost survival in the hypertonic seawater environment. The eel is a species that has been frequently used for osmoregulation research in laboratories worldwide. The eel possesses many advantages as an experimental animal for osmoregulation studies, one of which is its outstanding euryhalinity, which enables researchers to examine changes in the structure and function of the digestive tract after direct transfer from freshwater to seawater. In recent years, the molecular mechanisms of ion and water transport across epithelial cells (the transcellular route) and through tight junctions (the paracellular route) have been elucidated for the esophagus and intestine. Thanks to the rapid progress in analytical methods for genome databases on teleosts, including the eel, the molecular identities of transporters, channels, pumps and junctional proteins have been clarified at the isoform level. As 10 y have passed since the previous reviews on this subject, it seems relevant and timely to summarize recent progress in research on the molecular mechanisms of water and ion transport in the digestive tract in eels and to compare the mechanisms with those of other teleosts and mammals from comparative and evolutionary viewpoints. We also propose future directions for this research field to achieve integrative understanding of the role of the digestive tract in adaptation to seawater with regard to pathways/mechanisms including the paracellular route, divalent ion absorption, metabolon formation and cellular trafficking of transporters. Notably, some of these have already attracted practical attention in laboratories.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"10"},"PeriodicalIF":2.7,"publicationDate":"2021-06-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00175-x","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39014156","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}
Pub Date : 2021-05-27DOI: 10.1186/s40851-021-00176-w
Daniel Stec, Matteo Vecchi, Magdalena Dudziak, Paul J Bartels, Sara Calhim, Łukasz Michalczyk
The taxonomy of many groups of meiofauna is challenging due to their low number of diagnostic morphological characters and their small body size. Therefore, with the advent of molecular techniques that provide a new source of traits, many cryptic species have started to be discovered. Tardigrades are not an exception, and many once thought to be cosmopolitan taxa are being found to be complexes of phenotypically similar species. Macrobiotus pallarii Maucci, 1954 was originally described in South Italy and has been subsequently recorded in Europe, America, and Asia. This allegedly wide geographic range suggests that multiple species may be hidden under this name. Moreover, recently, genetic evidence to support this was put forward, and the Macrobiotus pallarii complex has been proposed to accommodate putative species related to M. pallarii. Here, we describe three new pseudocryptic species based on populations that would have been all classified as Macrobiotus pallarii if molecular methods were not employed. Using an integrative taxonomy approach, we analyzed animals and eggs from the topotypic population of Macrobiotus pallarii, together with four other populations of the complex. We recovered four distinct phylogenetic lineages that, despite the overlap of morphometric traits, can be separated phenotypically by subtle but discrete morphological characters. One lineage corresponds to Macrobiotus pallarii, whereas the other three are newly described as Macrobiotus margoae Stec, Vecchi & Bartels, sp. nov. from the USA, Macrobiotus ripperi Stec, Vecchi & Michalczyk, sp. nov. from Poland and Finland, and Macrobiotus pseudopallarii Stec, Vecchi & Michalczyk, sp. nov. from Montenegro. To facilitate species identification, we provide a dichotomous key for species of the M. pallarii complex. Delimitation of these pseudocryptic taxa highlights the need for an integrative approach to uncover the phylum's diversity in full.
{"title":"Integrative taxonomy resolves species identities within the Macrobiotus pallarii complex (Eutardigrada: Macrobiotidae).","authors":"Daniel Stec, Matteo Vecchi, Magdalena Dudziak, Paul J Bartels, Sara Calhim, Łukasz Michalczyk","doi":"10.1186/s40851-021-00176-w","DOIUrl":"https://doi.org/10.1186/s40851-021-00176-w","url":null,"abstract":"<p><p>The taxonomy of many groups of meiofauna is challenging due to their low number of diagnostic morphological characters and their small body size. Therefore, with the advent of molecular techniques that provide a new source of traits, many cryptic species have started to be discovered. Tardigrades are not an exception, and many once thought to be cosmopolitan taxa are being found to be complexes of phenotypically similar species. Macrobiotus pallarii Maucci, 1954 was originally described in South Italy and has been subsequently recorded in Europe, America, and Asia. This allegedly wide geographic range suggests that multiple species may be hidden under this name. Moreover, recently, genetic evidence to support this was put forward, and the Macrobiotus pallarii complex has been proposed to accommodate putative species related to M. pallarii. Here, we describe three new pseudocryptic species based on populations that would have been all classified as Macrobiotus pallarii if molecular methods were not employed. Using an integrative taxonomy approach, we analyzed animals and eggs from the topotypic population of Macrobiotus pallarii, together with four other populations of the complex. We recovered four distinct phylogenetic lineages that, despite the overlap of morphometric traits, can be separated phenotypically by subtle but discrete morphological characters. One lineage corresponds to Macrobiotus pallarii, whereas the other three are newly described as Macrobiotus margoae Stec, Vecchi & Bartels, sp. nov. from the USA, Macrobiotus ripperi Stec, Vecchi & Michalczyk, sp. nov. from Poland and Finland, and Macrobiotus pseudopallarii Stec, Vecchi & Michalczyk, sp. nov. from Montenegro. To facilitate species identification, we provide a dichotomous key for species of the M. pallarii complex. Delimitation of these pseudocryptic taxa highlights the need for an integrative approach to uncover the phylum's diversity in full.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"9"},"PeriodicalIF":2.7,"publicationDate":"2021-05-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00176-w","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38944347","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}
Pub Date : 2021-05-13DOI: 10.1186/s40851-021-00178-8
Minoru Moriyama, Kouji Yasuyama, Hideharu Numata
Insect eggshells must meet various demands of developing embryos. These demands sometimes conflict with each other; therefore, there are tradeoffs between eggshell properties, such as robustness and permeability. To meet these conflicting demands, particular eggshell structures have evolved in diverse insect species. Here, we report a rare eggshell structure found in the eggshell of a cicada, Cryptotympana facialis. This species has a prolonged egg period with embryonic diapause and a trait of humidity-inducible hatching, which would impose severe demands on the eggshell. We found that in eggs of this species, unlike many other insect eggs, a dedicated cleavage site, known as a hatching line, was formed not in the chorion but in the serosal cuticle. The hatching line was composed of a fine furrow accompanied by ridges on both sides. This furrow-ridge structure formed in the terminal phase of embryogenesis through the partial degradation of an initially thick and nearly flat cuticle layer. We showed that the permeability of the eggshell was low in the diapause stage, when the cuticle was thick, and increased with degradation of the serosal cuticle. We also demonstrated that the force required to cleave the eggshell was reduced after the formation of the hatching line. These results suggest that the establishment of the hatching line on the serosal cuticle enables flexible modification of eggshell properties during embryogenesis, and we predict that it is an adaptation to maximize the protective role of the shell during the long egg period while reducing the barrier to emerging nymphs at the time of hatching.
{"title":"The formation of a hatching line in the serosal cuticle confers multifaceted adaptive functions on the eggshell of a cicada.","authors":"Minoru Moriyama, Kouji Yasuyama, Hideharu Numata","doi":"10.1186/s40851-021-00178-8","DOIUrl":"https://doi.org/10.1186/s40851-021-00178-8","url":null,"abstract":"<p><p>Insect eggshells must meet various demands of developing embryos. These demands sometimes conflict with each other; therefore, there are tradeoffs between eggshell properties, such as robustness and permeability. To meet these conflicting demands, particular eggshell structures have evolved in diverse insect species. Here, we report a rare eggshell structure found in the eggshell of a cicada, Cryptotympana facialis. This species has a prolonged egg period with embryonic diapause and a trait of humidity-inducible hatching, which would impose severe demands on the eggshell. We found that in eggs of this species, unlike many other insect eggs, a dedicated cleavage site, known as a hatching line, was formed not in the chorion but in the serosal cuticle. The hatching line was composed of a fine furrow accompanied by ridges on both sides. This furrow-ridge structure formed in the terminal phase of embryogenesis through the partial degradation of an initially thick and nearly flat cuticle layer. We showed that the permeability of the eggshell was low in the diapause stage, when the cuticle was thick, and increased with degradation of the serosal cuticle. We also demonstrated that the force required to cleave the eggshell was reduced after the formation of the hatching line. These results suggest that the establishment of the hatching line on the serosal cuticle enables flexible modification of eggshell properties during embryogenesis, and we predict that it is an adaptation to maximize the protective role of the shell during the long egg period while reducing the barrier to emerging nymphs at the time of hatching.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"8"},"PeriodicalIF":2.7,"publicationDate":"2021-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00178-8","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38978215","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}
Pub Date : 2021-05-11DOI: 10.1186/s40851-021-00177-9
Miloš Vittori
Background: The study of joints in terrestrial arthropods can provide insights into the evolutionary optimization of contacting surfaces that slide without lubrication. This work reports on the structure of the joint between the propodus and the dactylus in terrestrial isopods, the most successful group of crustaceans on land, focusing on the woodlouse Porcellio scaber.
Methods: The joints were studied using fluorescence microscopy, 3D reconstruction, scanning electron microscopy and transmission electron microscopy. The obtained results were functionally interpreted using high-speed video recordings by analyzing the use of the joint during locomotion.
Results: In the joint, which allows the dactylus to move in a single plain, a semicircular process on the propodus fits into a groove on the dactylus and guides its movement. The sliding surfaces of the propodal process are textured in the form of parallel epicuticular ridges a few hundred nanometers thick. This texturing is selective: while the less heavily loaded surfaces are textured, the surfaces that support the isopod during standing and walking are smooth. In contrast, the groove on the dactylus is completely smooth. We found a similar surface texture in several other species of terrestrial isopods and one aquatic isopod.
Conclusions: The selective texturing of the joint may reduce wear by eliminating small particles. This effect of the ridges was confirmed using electron microscopy. The absence of ridges on heavily loaded surfaces may enhance the dissipation of forces in these regions.
{"title":"Structure of a hinge joint with textured sliding surfaces in terrestrial isopods (Crustacea: Isopoda: Oniscidea).","authors":"Miloš Vittori","doi":"10.1186/s40851-021-00177-9","DOIUrl":"https://doi.org/10.1186/s40851-021-00177-9","url":null,"abstract":"<p><strong>Background: </strong>The study of joints in terrestrial arthropods can provide insights into the evolutionary optimization of contacting surfaces that slide without lubrication. This work reports on the structure of the joint between the propodus and the dactylus in terrestrial isopods, the most successful group of crustaceans on land, focusing on the woodlouse Porcellio scaber.</p><p><strong>Methods: </strong>The joints were studied using fluorescence microscopy, 3D reconstruction, scanning electron microscopy and transmission electron microscopy. The obtained results were functionally interpreted using high-speed video recordings by analyzing the use of the joint during locomotion.</p><p><strong>Results: </strong>In the joint, which allows the dactylus to move in a single plain, a semicircular process on the propodus fits into a groove on the dactylus and guides its movement. The sliding surfaces of the propodal process are textured in the form of parallel epicuticular ridges a few hundred nanometers thick. This texturing is selective: while the less heavily loaded surfaces are textured, the surfaces that support the isopod during standing and walking are smooth. In contrast, the groove on the dactylus is completely smooth. We found a similar surface texture in several other species of terrestrial isopods and one aquatic isopod.</p><p><strong>Conclusions: </strong>The selective texturing of the joint may reduce wear by eliminating small particles. This effect of the ridges was confirmed using electron microscopy. The absence of ridges on heavily loaded surfaces may enhance the dissipation of forces in these regions.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"7"},"PeriodicalIF":2.7,"publicationDate":"2021-05-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00177-9","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"38971551","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}
Pub Date : 2021-04-12DOI: 10.1186/s40851-021-00172-0
Piotr Gąsiorek, Katarzyna Vončina, Joanna Ciosek, Mariana Veloso, Paulo Fontoura, Łukasz Michalczyk
Recent years have brought undeniable progress in tardigrade taxonomy, and speciose complexes were detected in a number of phylogenetic lineages. The family Echiniscidae is one such lineage; it is one of the most diverse groups of limno-terrestrial tardigrades and can be characterized as having achieved great evolutionary success. In this contribution, using populations representing several species that originated from the Indomalayan region, we reconstructed phylogenetic affinities within Nebularmis, a recently erected genus within the Echiniscus lineage. Nebularmis auratus sp. nov. and Nebularmis burmensis sp. nov. are described from the Eastern Yoma Mountains and the Shan Hills (Myanmar), Nebularmis bhutanensis sp. nov. is described from the Eastern Himalayas (Bhutan), and Nebularmis indicus sp. nov. is described from the foothills of the Western Ghats (Goa, India). Moreover, males are reported in populations of the last two species. All known members of the genus can be phenotypically differentiated based on minute details of their dorsal sculpture and claws. Moreover, a very wide tropical distribution is demonstrated for Nebularmis cirinoi, recorded for the first time from islands of the Malay Archipelago. Furthemore, novel morphological, genetic, and geographic data allowed for the clarification of the generic diagnosis. Currently available data favor a scenario under which Nebularmis evolved in Southeast Asia and later dispersed to other regions of the globe.
{"title":"New Indomalayan Nebularmis species (Heterotardigrada: Echiniscidae) provoke a discussion on its intrageneric diversity.","authors":"Piotr Gąsiorek, Katarzyna Vončina, Joanna Ciosek, Mariana Veloso, Paulo Fontoura, Łukasz Michalczyk","doi":"10.1186/s40851-021-00172-0","DOIUrl":"10.1186/s40851-021-00172-0","url":null,"abstract":"<p><p>Recent years have brought undeniable progress in tardigrade taxonomy, and speciose complexes were detected in a number of phylogenetic lineages. The family Echiniscidae is one such lineage; it is one of the most diverse groups of limno-terrestrial tardigrades and can be characterized as having achieved great evolutionary success. In this contribution, using populations representing several species that originated from the Indomalayan region, we reconstructed phylogenetic affinities within Nebularmis, a recently erected genus within the Echiniscus lineage. Nebularmis auratus sp. nov. and Nebularmis burmensis sp. nov. are described from the Eastern Yoma Mountains and the Shan Hills (Myanmar), Nebularmis bhutanensis sp. nov. is described from the Eastern Himalayas (Bhutan), and Nebularmis indicus sp. nov. is described from the foothills of the Western Ghats (Goa, India). Moreover, males are reported in populations of the last two species. All known members of the genus can be phenotypically differentiated based on minute details of their dorsal sculpture and claws. Moreover, a very wide tropical distribution is demonstrated for Nebularmis cirinoi, recorded for the first time from islands of the Malay Archipelago. Furthemore, novel morphological, genetic, and geographic data allowed for the clarification of the generic diagnosis. Currently available data favor a scenario under which Nebularmis evolved in Southeast Asia and later dispersed to other regions of the globe.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"6"},"PeriodicalIF":2.7,"publicationDate":"2021-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8040243/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"25584745","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}
Pub Date : 2021-03-25DOI: 10.1186/s40851-021-00174-y
Mikołaj Kaczmarski, Jan M Kaczmarek, Łukasz Jankowiak, Krzysztof Kolenda, Piotr Tryjanowski
Introduction: Despite the growing number of studies describing digit ratio patterns in tetrapods, knowledge concerning certain basic issues is still scarce. In lower vertebrates such as tailless amphibians (Anura), the numbering of individual fingers on the forelimbs and their homology with the fingers of other vertebrates pose an unsolved problem. Based on reviewed data on anuran limb development, we argue that the correct finger numbering scheme should be based on the assumption that the first finger, not the fifth finger, was reduced on the forelimbs. We analyzed the digit ratio in the common toad (Bufo bufo, Bufonidae), a species characterized by well-developed sexual dimorphism whereby females are larger than males, using both numbering schemes present in the literature.
Results: We found that the digit ratio on hindlimbs differed significantly between the sexes only in the cases of left 2D:3D, with lower digit ratios in females, and of left 3D:4D, with lower digit ratios in males. We found that sex was the only significant variable for forelimbs, differentiating 2D:3D on the left forelimb, with lower digit ratios in females; 2D:4D on the right forelimb, with lower digit ratios in males; and 3D:4D on both forelimbs, with lower digit ratios in males. These results relate to variant II reflecting the hypothesis that the first digit was reduced during phylogenesis. There was no relationship between the body size (SVL) of individuals and any digit ratio, excluding 2D:4D on the right forelimbs in models with age variables. Additionally, for a subset of data where individual age was known, the models indicated that age was linked to significant differences in 2D:4D and 3D:4D on the left hindlimbs, while age, SVL, and sex influenced 2D:4D on the right forelimbs.
Conclusion: We emphasize the importance of the problem of the correct numbering of forelimb digits in Anura and, under the assumption that it was the fifth digit that was reduced, argue that earlier results on digit ratio in this group should be interpreted with caution. The detected relationship between digit ratio and age in amphibians expands our knowledge, indicating that the age of individuals should be included in future digit ratio studies. This relationship may also apply to studies using digit ratio as a noninvasive indicator of endocrine disruption in amphibians.
{"title":"Digit ratio in the common toad Bufo bufo: the effects of reduced fingers and of age dependency.","authors":"Mikołaj Kaczmarski, Jan M Kaczmarek, Łukasz Jankowiak, Krzysztof Kolenda, Piotr Tryjanowski","doi":"10.1186/s40851-021-00174-y","DOIUrl":"10.1186/s40851-021-00174-y","url":null,"abstract":"<p><strong>Introduction: </strong>Despite the growing number of studies describing digit ratio patterns in tetrapods, knowledge concerning certain basic issues is still scarce. In lower vertebrates such as tailless amphibians (Anura), the numbering of individual fingers on the forelimbs and their homology with the fingers of other vertebrates pose an unsolved problem. Based on reviewed data on anuran limb development, we argue that the correct finger numbering scheme should be based on the assumption that the first finger, not the fifth finger, was reduced on the forelimbs. We analyzed the digit ratio in the common toad (Bufo bufo, Bufonidae), a species characterized by well-developed sexual dimorphism whereby females are larger than males, using both numbering schemes present in the literature.</p><p><strong>Results: </strong>We found that the digit ratio on hindlimbs differed significantly between the sexes only in the cases of left 2D:3D, with lower digit ratios in females, and of left 3D:4D, with lower digit ratios in males. We found that sex was the only significant variable for forelimbs, differentiating 2D:3D on the left forelimb, with lower digit ratios in females; 2D:4D on the right forelimb, with lower digit ratios in males; and 3D:4D on both forelimbs, with lower digit ratios in males. These results relate to variant II reflecting the hypothesis that the first digit was reduced during phylogenesis. There was no relationship between the body size (SVL) of individuals and any digit ratio, excluding 2D:4D on the right forelimbs in models with age variables. Additionally, for a subset of data where individual age was known, the models indicated that age was linked to significant differences in 2D:4D and 3D:4D on the left hindlimbs, while age, SVL, and sex influenced 2D:4D on the right forelimbs.</p><p><strong>Conclusion: </strong>We emphasize the importance of the problem of the correct numbering of forelimb digits in Anura and, under the assumption that it was the fifth digit that was reduced, argue that earlier results on digit ratio in this group should be interpreted with caution. The detected relationship between digit ratio and age in amphibians expands our knowledge, indicating that the age of individuals should be included in future digit ratio studies. This relationship may also apply to studies using digit ratio as a noninvasive indicator of endocrine disruption in amphibians.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"5"},"PeriodicalIF":2.7,"publicationDate":"2021-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7992345/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"25516851","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}
Background: Many animals switch between asexual and sexual reproduction in nature. We previously established a system for the sexual induction of planarian Dugesia ryukyuensis by feeding asexual planarians with minced sexual planarians. We identified DL-tryptophan (Trp) as one of the sex-inducing substances. DL-Trp can induce ovarian development, the first and essential step of sexual induction. D-Trp must act as a principal bioactive compound in terms of ovarian development, because the ovary-inducing activity of D-Trp was 500 times more potent than that of L-Trp. However, how Trp controls sexual induction is still unknown.
Results: In this study, qRT-PCR analyses suggested that the putative amino acid transporter gene Dr-SLC38A9 is highly expressed in sexual worms, especially in the yolk glands. In situ hybridization analyses showed that Dr-SLC38A9 is expressed in the ovarian primordia of asexual worms and in the mature ovaries, testes, and yolk glands of sexual worms. In addition, Dr-SLC38A9 RNA interference during sexual induction resulted in the suppression of the development of reproductive organs. These results suggest that Dr-SLC38A9 is involved in the development of these organs. Moreover, we demonstrated that the reproductive organ-specific expression of Dr-SLC38A9 is enhanced by the addition of D-Trp.
Conclusion: We propose that D-Trp activates the expression of Dr-SLC38A9 to promote sexual induction in the planarian D. ryukyuensis.
{"title":"D-Tryptophan enhances the reproductive organ-specific expression of the amino acid transporter homolog Dr-SLC38A9 involved in the sexual induction of planarian Dugesia ryukyuensis.","authors":"Takanobu Maezawa, Masaki Ishikawa, Kiyono Sekii, Go Nagamatsu, Ryohei Furukawa, Kazuya Kobayashi","doi":"10.1186/s40851-021-00173-z","DOIUrl":"https://doi.org/10.1186/s40851-021-00173-z","url":null,"abstract":"<p><strong>Background: </strong>Many animals switch between asexual and sexual reproduction in nature. We previously established a system for the sexual induction of planarian Dugesia ryukyuensis by feeding asexual planarians with minced sexual planarians. We identified DL-tryptophan (Trp) as one of the sex-inducing substances. DL-Trp can induce ovarian development, the first and essential step of sexual induction. D-Trp must act as a principal bioactive compound in terms of ovarian development, because the ovary-inducing activity of D-Trp was 500 times more potent than that of L-Trp. However, how Trp controls sexual induction is still unknown.</p><p><strong>Results: </strong>In this study, qRT-PCR analyses suggested that the putative amino acid transporter gene Dr-SLC38A9 is highly expressed in sexual worms, especially in the yolk glands. In situ hybridization analyses showed that Dr-SLC38A9 is expressed in the ovarian primordia of asexual worms and in the mature ovaries, testes, and yolk glands of sexual worms. In addition, Dr-SLC38A9 RNA interference during sexual induction resulted in the suppression of the development of reproductive organs. These results suggest that Dr-SLC38A9 is involved in the development of these organs. Moreover, we demonstrated that the reproductive organ-specific expression of Dr-SLC38A9 is enhanced by the addition of D-Trp.</p><p><strong>Conclusion: </strong>We propose that D-Trp activates the expression of Dr-SLC38A9 to promote sexual induction in the planarian D. ryukyuensis.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"4"},"PeriodicalIF":2.7,"publicationDate":"2021-03-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00173-z","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"25498455","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}
Quaternary environmental changes fundamentally influenced the genetic diversity of temperate-zone terrestrial animals, including those in the Japanese Archipelago. The genetic diversity of present-day populations is taxon- and region-specific, but its determinants are poorly understood. Here, we analyzed cytochrome b gene (Cytb) sequences (1140 bp) of mitochondrial DNA (mtDNA) to elucidate the factors determining the genetic variation in three species of large moles: Mogera imaizumii and Mogera wogura, which occur in central and southern mainland Japan (Honshu, Shikoku, and Kyushu), and Mogera robusta, which occurs on the nearby Asian continent. Network construction with the Cytb sequences revealed 10 star-shaped clusters with apparent geographic affinity. Mismatch distribution analysis showed that modes of pairwise nucleotide differences (τ values) were grouped into five classes in terms of the level, implying the occurrence of five stages for rapid expansion. It is conceivable that severe cold periods and subsequent warm periods during the late Quaternary were responsible for the population expansion events. The first and third oldest events included island-derived haplotypes, indicative of the involvement of land bridge formation between remote islands, hence suggesting an association of the ends of the penultimate (PGM, ca. 130,000 years ago) and last (LGM, ca. 15,000 years ago) glacial maxima, respectively. Since the third event was followed by the fourth, it is plausible that the termination of the Younger Dryas and subsequent abrupt warming ca. 11,500 years ago facilitated the fourth expansion event. The second event most likely corresponded to early marine isotope stage (MIS) 3 (ca. 53,000 years ago) when the glaciation and subsequent warming period were predicted to have influenced biodiversity. Utilization of the critical times of 130,000, 53,000, 15,000, and 11,500 years ago as calibration points yielded evolutionary rates of 0.03, 0.045, 0.10 and 0.10 substitutions/site/million years, respectively, showing a time-dependent manner whose pattern was similar to that seen in small rodents reported in our previous studies. The age of the fifth expansion event was calculated to be 5800 years ago with a rate of 0.10 substitutions/site/million years ago during the mid-Holocene, suggestive of the influence of humans or other unspecified reasons, such as the Jomon marine transgression.
{"title":"Influence of Quaternary environmental changes on mole populations inferred from mitochondrial sequences and evolutionary rate estimation.","authors":"Azusa Nakamoto, Masashi Harada, Reiko Mitsuhashi, Kimiyuki Tsuchiya, Alexey P Kryukov, Akio Shinohara, Hitoshi Suzuki","doi":"10.1186/s40851-021-00169-9","DOIUrl":"https://doi.org/10.1186/s40851-021-00169-9","url":null,"abstract":"<p><p>Quaternary environmental changes fundamentally influenced the genetic diversity of temperate-zone terrestrial animals, including those in the Japanese Archipelago. The genetic diversity of present-day populations is taxon- and region-specific, but its determinants are poorly understood. Here, we analyzed cytochrome b gene (Cytb) sequences (1140 bp) of mitochondrial DNA (mtDNA) to elucidate the factors determining the genetic variation in three species of large moles: Mogera imaizumii and Mogera wogura, which occur in central and southern mainland Japan (Honshu, Shikoku, and Kyushu), and Mogera robusta, which occurs on the nearby Asian continent. Network construction with the Cytb sequences revealed 10 star-shaped clusters with apparent geographic affinity. Mismatch distribution analysis showed that modes of pairwise nucleotide differences (τ values) were grouped into five classes in terms of the level, implying the occurrence of five stages for rapid expansion. It is conceivable that severe cold periods and subsequent warm periods during the late Quaternary were responsible for the population expansion events. The first and third oldest events included island-derived haplotypes, indicative of the involvement of land bridge formation between remote islands, hence suggesting an association of the ends of the penultimate (PGM, ca. 130,000 years ago) and last (LGM, ca. 15,000 years ago) glacial maxima, respectively. Since the third event was followed by the fourth, it is plausible that the termination of the Younger Dryas and subsequent abrupt warming ca. 11,500 years ago facilitated the fourth expansion event. The second event most likely corresponded to early marine isotope stage (MIS) 3 (ca. 53,000 years ago) when the glaciation and subsequent warming period were predicted to have influenced biodiversity. Utilization of the critical times of 130,000, 53,000, 15,000, and 11,500 years ago as calibration points yielded evolutionary rates of 0.03, 0.045, 0.10 and 0.10 substitutions/site/million years, respectively, showing a time-dependent manner whose pattern was similar to that seen in small rodents reported in our previous studies. The age of the fifth expansion event was calculated to be 5800 years ago with a rate of 0.10 substitutions/site/million years ago during the mid-Holocene, suggestive of the influence of humans or other unspecified reasons, such as the Jomon marine transgression.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"2"},"PeriodicalIF":2.7,"publicationDate":"2021-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00169-9","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"25371521","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}
Vertebrate extraocular muscles (EOMs) function in eye movements. The EOMs of modern jawed vertebrates consist primarily of four recti and two oblique muscles innervated by three cranial nerves. The developmental mechanisms underlying the establishment of this complex and the evolutionarily conserved pattern of EOMs are unknown. Chondrichthyan early embryos develop three pairs of overt epithelial coeloms called head cavities (HCs) in the head mesoderm, and each HC is believed to differentiate into a discrete subset of EOMs. However, no direct evidence of these cell fates has been provided due to the technical difficulty of lineage tracing experiments in chondrichthyans. Here, we set up an in ovo manipulation system for embryos of the cloudy catshark Scyliorhinus torazame and labeled the epithelial cells of each HC with lipophilic fluorescent dyes. This experimental system allowed us to trace the cell lineage of EOMs with the highest degree of detail and reproducibility to date. We confirmed that the HCs are indeed primordia of EOMs but showed that the morphological pattern of shark EOMs is not solely dependent on the early pattern of the head mesoderm, which transiently appears as tripartite HCs along the simple anteroposterior axis. Moreover, we found that one of the HCs gives rise to tendon progenitor cells of the EOMs, which is an exceptional condition in our previous understanding of head muscles; the tendons associated with head muscles have generally been supposed to be derived from cranial neural crest (CNC) cells, another source of vertebrate head mesenchyme. Based on interspecies comparisons, the developmental environment is suggested to be significantly different between the two ends of the rectus muscles, and this difference is suggested to be evolutionarily conserved in jawed vertebrates. We propose that the mesenchymal interface (head mesoderm vs CNC) in the environment of developing EOM is required to determine the processes of the proximodistal axis of rectus components of EOMs.
{"title":"Developmental fates of shark head cavities reveal mesodermal contributions to tendon progenitor cells in extraocular muscles.","authors":"Shunya Kuroda, Noritaka Adachi, Rie Kusakabe, Shigeru Kuratani","doi":"10.1186/s40851-021-00170-2","DOIUrl":"https://doi.org/10.1186/s40851-021-00170-2","url":null,"abstract":"<p><p>Vertebrate extraocular muscles (EOMs) function in eye movements. The EOMs of modern jawed vertebrates consist primarily of four recti and two oblique muscles innervated by three cranial nerves. The developmental mechanisms underlying the establishment of this complex and the evolutionarily conserved pattern of EOMs are unknown. Chondrichthyan early embryos develop three pairs of overt epithelial coeloms called head cavities (HCs) in the head mesoderm, and each HC is believed to differentiate into a discrete subset of EOMs. However, no direct evidence of these cell fates has been provided due to the technical difficulty of lineage tracing experiments in chondrichthyans. Here, we set up an in ovo manipulation system for embryos of the cloudy catshark Scyliorhinus torazame and labeled the epithelial cells of each HC with lipophilic fluorescent dyes. This experimental system allowed us to trace the cell lineage of EOMs with the highest degree of detail and reproducibility to date. We confirmed that the HCs are indeed primordia of EOMs but showed that the morphological pattern of shark EOMs is not solely dependent on the early pattern of the head mesoderm, which transiently appears as tripartite HCs along the simple anteroposterior axis. Moreover, we found that one of the HCs gives rise to tendon progenitor cells of the EOMs, which is an exceptional condition in our previous understanding of head muscles; the tendons associated with head muscles have generally been supposed to be derived from cranial neural crest (CNC) cells, another source of vertebrate head mesenchyme. Based on interspecies comparisons, the developmental environment is suggested to be significantly different between the two ends of the rectus muscles, and this difference is suggested to be evolutionarily conserved in jawed vertebrates. We propose that the mesenchymal interface (head mesoderm vs CNC) in the environment of developing EOM is required to determine the processes of the proximodistal axis of rectus components of EOMs.</p>","PeriodicalId":54280,"journal":{"name":"Zoological Letters","volume":"7 1","pages":"3"},"PeriodicalIF":2.7,"publicationDate":"2021-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1186/s40851-021-00170-2","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"25375152","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}