Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage
Abstract Key changes in ecological niche space are often critical to understanding how lineages diversify during adaptive radiations. However, the converse, or understanding why some lineages are depauperate and relictual, is more challenging, as many factors may constrain niche evolution. In the ca...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Wiley
2021-02-01
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| Series: | Evolutionary Applications |
| Subjects: | |
| Online Access: | https://doi.org/10.1111/eva.13120 |
| _version_ | 1818923853963853824 |
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| author | Sean D. Schoville Sabrina Simon Ming Bai Zachary Beethem Roman Y. Dudko Monika J. B. Eberhard Paul B. Frandsen Simon C. Küpper Ryuichiro Machida Max Verheij Peter C. Willadsen Xin Zhou Benjamin Wipfler |
| author_facet | Sean D. Schoville Sabrina Simon Ming Bai Zachary Beethem Roman Y. Dudko Monika J. B. Eberhard Paul B. Frandsen Simon C. Küpper Ryuichiro Machida Max Verheij Peter C. Willadsen Xin Zhou Benjamin Wipfler |
| author_sort | Sean D. Schoville |
| collection | DOAJ |
| description | Abstract Key changes in ecological niche space are often critical to understanding how lineages diversify during adaptive radiations. However, the converse, or understanding why some lineages are depauperate and relictual, is more challenging, as many factors may constrain niche evolution. In the case of the insect order Grylloblattodea, highly conserved thermal breadth is assumed to be closely tied to their relictual status, but has not been formerly tested. Here, we investigate whether evolutionary constraints in the physiological tolerance of temperature can help explain relictualism in this lineage. Using a comparative transcriptomics approach, we investigate gene expression following acute heat and cold stress across members of Grylloblattodea and their sister group, Mantophasmatodea. We additionally examine patterns of protein evolution, to identify candidate genes of positive selection. We demonstrate that cold specialization in Grylloblattodea has been accompanied by the loss of the inducible heat shock response under both acute heat and cold stress. Additionally, there is widespread evidence of selection on protein‐coding genes consistent with evolutionary constraints due to cold specialization. This includes positive selection on genes involved in trehalose transport, metabolic function, mitochondrial function, oxygen reduction, oxidative stress, and protein synthesis. These patterns of molecular adaptation suggest that Grylloblattodea have undergone evolutionary trade‐offs to survive in cold habitats and should be considered highly vulnerable to climate change. Finally, our transcriptomic data provide a robust backbone phylogeny for generic relationships within Grylloblattodea and Mantophasmatodea. Major phylogenetic splits in each group relate to arid conditions driving biogeographical patterns, with support for a sister‐group relationship between North American Grylloblatta and Altai‐Sayan Grylloblattella, and a range disjunction in Namibia splitting major clades within Mantophasmatodea. |
| first_indexed | 2024-12-20T02:16:03Z |
| format | Article |
| id | doaj.art-4e920a86d3f842c6992495d3bbd24e99 |
| institution | Directory Open Access Journal |
| issn | 1752-4571 |
| language | English |
| last_indexed | 2024-12-20T02:16:03Z |
| publishDate | 2021-02-01 |
| publisher | Wiley |
| record_format | Article |
| series | Evolutionary Applications |
| spelling | doaj.art-4e920a86d3f842c6992495d3bbd24e992022-12-21T19:56:56ZengWileyEvolutionary Applications1752-45712021-02-0114236038210.1111/eva.13120Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineageSean D. Schoville0Sabrina Simon1Ming Bai2Zachary Beethem3Roman Y. Dudko4Monika J. B. Eberhard5Paul B. Frandsen6Simon C. Küpper7Ryuichiro Machida8Max Verheij9Peter C. Willadsen10Xin Zhou11Benjamin Wipfler12Department of Entomology University of Wisconsin‐Madison Madison WI USABiosystematics Group Wageningen University & Research PB Wageningen The NetherlandsKey Laboratory of Zoological Systematics and Evolution Institute of Zoology Chinese Academy of Sciences Beijing ChinaDepartment of Entomology University of Wisconsin‐Madison Madison WI USAInstitute of Systematics and Ecology of Animals Siberian Branch of the Russian Academy of Sciences Novosibirsk RussiaZoological Institute and Museum General Zoology and Zoological Systematics University of Greifswald Greifswald GermanyDepartment of Plant & Wildlife Sciences Brigham Young University Provo UT USAZoological Institute and Museum General Zoology and Zoological Systematics University of Greifswald Greifswald GermanySugadaira Research Station Mountain Science Center University of Tsukuba Ueda, Nagano JapanBiosystematics Group Wageningen University & Research PB Wageningen The NetherlandsDepartment of Entomology University of Wisconsin‐Madison Madison WI USADepartment of Entomology College of Plant Protection China Agricultural University Beijing ChinaZoologisches Forschungsmuseum Alexander Koenig Bonn GermanyAbstract Key changes in ecological niche space are often critical to understanding how lineages diversify during adaptive radiations. However, the converse, or understanding why some lineages are depauperate and relictual, is more challenging, as many factors may constrain niche evolution. In the case of the insect order Grylloblattodea, highly conserved thermal breadth is assumed to be closely tied to their relictual status, but has not been formerly tested. Here, we investigate whether evolutionary constraints in the physiological tolerance of temperature can help explain relictualism in this lineage. Using a comparative transcriptomics approach, we investigate gene expression following acute heat and cold stress across members of Grylloblattodea and their sister group, Mantophasmatodea. We additionally examine patterns of protein evolution, to identify candidate genes of positive selection. We demonstrate that cold specialization in Grylloblattodea has been accompanied by the loss of the inducible heat shock response under both acute heat and cold stress. Additionally, there is widespread evidence of selection on protein‐coding genes consistent with evolutionary constraints due to cold specialization. This includes positive selection on genes involved in trehalose transport, metabolic function, mitochondrial function, oxygen reduction, oxidative stress, and protein synthesis. These patterns of molecular adaptation suggest that Grylloblattodea have undergone evolutionary trade‐offs to survive in cold habitats and should be considered highly vulnerable to climate change. Finally, our transcriptomic data provide a robust backbone phylogeny for generic relationships within Grylloblattodea and Mantophasmatodea. Major phylogenetic splits in each group relate to arid conditions driving biogeographical patterns, with support for a sister‐group relationship between North American Grylloblatta and Altai‐Sayan Grylloblattella, and a range disjunction in Namibia splitting major clades within Mantophasmatodea.https://doi.org/10.1111/eva.13120adaptationgene regulationGrylloblattodeainsect phylogenomicsniche conservatismprotein evolution |
| spellingShingle | Sean D. Schoville Sabrina Simon Ming Bai Zachary Beethem Roman Y. Dudko Monika J. B. Eberhard Paul B. Frandsen Simon C. Küpper Ryuichiro Machida Max Verheij Peter C. Willadsen Xin Zhou Benjamin Wipfler Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage Evolutionary Applications adaptation gene regulation Grylloblattodea insect phylogenomics niche conservatism protein evolution |
| title | Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| title_full | Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| title_fullStr | Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| title_full_unstemmed | Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| title_short | Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| title_sort | comparative transcriptomics of ice crawlers demonstrates cold specialization constrains niche evolution in a relict lineage |
| topic | adaptation gene regulation Grylloblattodea insect phylogenomics niche conservatism protein evolution |
| url | https://doi.org/10.1111/eva.13120 |
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