Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques
Abstract Background Novel feeding adaptations often facilitate adaptive radiation and diversification. But the evolutionary origins of such feeding adaptations can be puzzling if they require concordant change in multiple component parts. Pelagic, heterorhabdid copepods (Calanoida) exhibit diverse f...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2019-08-01
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| Series: | Frontiers in Zoology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12983-019-0308-y |
| _version_ | 1818339791385657344 |
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| author | Tomonari Kaji Chihong Song Kazuyoshi Murata Shigenori Nonaka Kota Ogawa Yusuke Kondo Susumu Ohtsuka A. Richard Palmer |
| author_facet | Tomonari Kaji Chihong Song Kazuyoshi Murata Shigenori Nonaka Kota Ogawa Yusuke Kondo Susumu Ohtsuka A. Richard Palmer |
| author_sort | Tomonari Kaji |
| collection | DOAJ |
| description | Abstract Background Novel feeding adaptations often facilitate adaptive radiation and diversification. But the evolutionary origins of such feeding adaptations can be puzzling if they require concordant change in multiple component parts. Pelagic, heterorhabdid copepods (Calanoida) exhibit diverse feeding behaviors that range from simple particle feeding to a highly specialized form of carnivory involving piercing mouthparts that likely inject venom. We review the evolutionary history of heterorhabdid copepods and add new high-resolution, 3D anatomical analyses of the muscular system, glands and gland openings associated with this remarkable evolutionary transformation. Results We examined four heterorhabdid copepods with different feeding modes: one primitive particle-feeder (Disseta palumbii), one derived and specialized carnivore (Heterorhabdus subspinifrons), and two intermediate taxa (Mesorhabdus gracilis and Heterostylites longicornis). We used two advanced, high-resolution microscopic techniques — serial block-face scanning electron microscopy and two-photon excitation microscopy — to visualize mouthpart form and internal anatomy at unprecedented nanometer resolution. Interactive 3D graphical visualizations allowed putative homologues of muscles and gland cells to be identified with confidence and traced across the evolutionary transformation from particle feeding to piercing carnivory. Notable changes included: a) addition of new gland cells, b) enlargement of some (venom producing?) glands, c) repositioning of gland openings associated with hollow piercing fangs on the mandibles, d) repurposing of some mandibular-muscle function to include gland-squeezing, and e) addition of new muscles that may aid venom injection exclusively in the most specialized piercing species. In addition, live video recording of all four species revealed mandibular blade movements coupled to cyclic contraction of some muscles connected to the esophagus. These behavioral and 3D morphological observations revealed a novel injection system in H. subspinifrons associated with piercing (envenomating?) carnivory. Conclusions Collectively, these results suggest that subtle changes in mandibular tooth form, and muscle and gland form and location, facilitated the evolution of a novel, piercing mode of feeding that accelerated diversification of the genus Heterorhabdus. They also highlight the value of interactive 3D animations for understanding evolutionary transformations of complex, multicomponent morphological systems. |
| first_indexed | 2024-12-13T15:32:37Z |
| format | Article |
| id | doaj.art-2ab917f08ba5495da213439563d56c45 |
| institution | Directory Open Access Journal |
| issn | 1742-9994 |
| language | English |
| last_indexed | 2024-12-13T15:32:37Z |
| publishDate | 2019-08-01 |
| publisher | BMC |
| record_format | Article |
| series | Frontiers in Zoology |
| spelling | doaj.art-2ab917f08ba5495da213439563d56c452022-12-21T23:40:08ZengBMCFrontiers in Zoology1742-99942019-08-0116111410.1186/s12983-019-0308-yEvolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniquesTomonari Kaji0Chihong Song1Kazuyoshi Murata2Shigenori Nonaka3Kota Ogawa4Yusuke Kondo5Susumu Ohtsuka6A. Richard Palmer7Department of Biological Sciences, University of AlbertaNational Institute for Physiological SciencesNational Institute for Physiological SciencesNational Institute for Basic BiologyBiosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu UniversitySetouchi Field Science Center, Graduate School of Integrated Sciences for Life, Hiroshima UniversitySetouchi Field Science Center, Graduate School of Integrated Sciences for Life, Hiroshima UniversityDepartment of Biological Sciences, University of AlbertaAbstract Background Novel feeding adaptations often facilitate adaptive radiation and diversification. But the evolutionary origins of such feeding adaptations can be puzzling if they require concordant change in multiple component parts. Pelagic, heterorhabdid copepods (Calanoida) exhibit diverse feeding behaviors that range from simple particle feeding to a highly specialized form of carnivory involving piercing mouthparts that likely inject venom. We review the evolutionary history of heterorhabdid copepods and add new high-resolution, 3D anatomical analyses of the muscular system, glands and gland openings associated with this remarkable evolutionary transformation. Results We examined four heterorhabdid copepods with different feeding modes: one primitive particle-feeder (Disseta palumbii), one derived and specialized carnivore (Heterorhabdus subspinifrons), and two intermediate taxa (Mesorhabdus gracilis and Heterostylites longicornis). We used two advanced, high-resolution microscopic techniques — serial block-face scanning electron microscopy and two-photon excitation microscopy — to visualize mouthpart form and internal anatomy at unprecedented nanometer resolution. Interactive 3D graphical visualizations allowed putative homologues of muscles and gland cells to be identified with confidence and traced across the evolutionary transformation from particle feeding to piercing carnivory. Notable changes included: a) addition of new gland cells, b) enlargement of some (venom producing?) glands, c) repositioning of gland openings associated with hollow piercing fangs on the mandibles, d) repurposing of some mandibular-muscle function to include gland-squeezing, and e) addition of new muscles that may aid venom injection exclusively in the most specialized piercing species. In addition, live video recording of all four species revealed mandibular blade movements coupled to cyclic contraction of some muscles connected to the esophagus. These behavioral and 3D morphological observations revealed a novel injection system in H. subspinifrons associated with piercing (envenomating?) carnivory. Conclusions Collectively, these results suggest that subtle changes in mandibular tooth form, and muscle and gland form and location, facilitated the evolution of a novel, piercing mode of feeding that accelerated diversification of the genus Heterorhabdus. They also highlight the value of interactive 3D animations for understanding evolutionary transformations of complex, multicomponent morphological systems.http://link.springer.com/article/10.1186/s12983-019-0308-yFeeding strategiesFunctional morphologyMorphological noveltyAppendage innovationCrustaceaCalanoida |
| spellingShingle | Tomonari Kaji Chihong Song Kazuyoshi Murata Shigenori Nonaka Kota Ogawa Yusuke Kondo Susumu Ohtsuka A. Richard Palmer Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques Frontiers in Zoology Feeding strategies Functional morphology Morphological novelty Appendage innovation Crustacea Calanoida |
| title | Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques |
| title_full | Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques |
| title_fullStr | Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques |
| title_full_unstemmed | Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques |
| title_short | Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques |
| title_sort | evolutionary transformation of mouthparts from particle feeding to piercing carnivory in viper copepods review and 3d analyses of a key innovation using advanced imaging techniques |
| topic | Feeding strategies Functional morphology Morphological novelty Appendage innovation Crustacea Calanoida |
| url | http://link.springer.com/article/10.1186/s12983-019-0308-y |
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