Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders
Abstract Background A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to in...
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| Format: | Article |
| Language: | English |
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BMC
2021-03-01
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| Series: | BMC Ecology and Evolution |
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| Online Access: | https://doi.org/10.1186/s12862-021-01779-9 |
| _version_ | 1818681814917578752 |
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| author | Cory A. Berger Michael S. Brewer Nobuaki Kono Hiroyuki Nakamura Kazuharu Arakawa Susan R. Kennedy Hannah M. Wood Seira A. Adams Rosemary G. Gillespie |
| author_facet | Cory A. Berger Michael S. Brewer Nobuaki Kono Hiroyuki Nakamura Kazuharu Arakawa Susan R. Kennedy Hannah M. Wood Seira A. Adams Rosemary G. Gillespie |
| author_sort | Cory A. Berger |
| collection | DOAJ |
| description | Abstract Background A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages. Results The cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae. Conclusions Our results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors. |
| first_indexed | 2024-12-17T10:08:56Z |
| format | Article |
| id | doaj.art-1a678f6b60b441539f41b8d2f4135e4e |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-12-17T10:08:56Z |
| publishDate | 2021-03-01 |
| publisher | BMC |
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| series | BMC Ecology and Evolution |
| spelling | doaj.art-1a678f6b60b441539f41b8d2f4135e4e2022-12-21T21:53:04ZengBMCBMC Ecology and Evolution2730-71822021-03-0121111710.1186/s12862-021-01779-9Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spidersCory A. Berger0Michael S. Brewer1Nobuaki Kono2Hiroyuki Nakamura3Kazuharu Arakawa4Susan R. Kennedy5Hannah M. Wood6Seira A. Adams7Rosemary G. Gillespie8Department of Environmental Science, Policy and Management, University of California, BerkeleyDepartment of Biology, N1088 Howell Science Complex, East Carolina UniversityInstitute for Advanced Biosciences, Keio UniversityEnzyme Research Team, RIKEN Center for Sustainable Resource ScienceInstitute for Advanced Biosciences, Keio UniversityBiodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Graduate UniversitySmithsonian Institution, Entomology, MRC105Department of Environmental Science, Policy and Management, University of California, BerkeleyDepartment of Environmental Science, Policy and Management, University of California, BerkeleyAbstract Background A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages. Results The cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae. Conclusions Our results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors.https://doi.org/10.1186/s12862-021-01779-9ConvergenceTetragnathaSpidroinsWeb lossTranscriptomicsSelection |
| spellingShingle | Cory A. Berger Michael S. Brewer Nobuaki Kono Hiroyuki Nakamura Kazuharu Arakawa Susan R. Kennedy Hannah M. Wood Seira A. Adams Rosemary G. Gillespie Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders BMC Ecology and Evolution Convergence Tetragnatha Spidroins Web loss Transcriptomics Selection |
| title | Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders |
| title_full | Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders |
| title_fullStr | Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders |
| title_full_unstemmed | Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders |
| title_short | Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders |
| title_sort | shifts in morphology gene expression and selection underlie web loss in hawaiian tetragnatha spiders |
| topic | Convergence Tetragnatha Spidroins Web loss Transcriptomics Selection |
| url | https://doi.org/10.1186/s12862-021-01779-9 |
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