The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea)
The relatively small insect order Mantodea (praying mantises) is comprised of approximately 2,366 described species distributed in 436 genera. Members of the group occupy diverse habitats and are distributed across the globe, though their greatest numbers and diversity are concentrated primarily in...
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2007
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Dictyoptera Mantodea Biogeography Systematics mantis praying mantis Auditory evolution Insect Biology |
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Dictyoptera Mantodea Biogeography Systematics mantis praying mantis Auditory evolution Insect Biology Svenson, Gavin John The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
description |
The relatively small insect order Mantodea (praying mantises) is comprised of approximately 2,366 described species distributed in 436 genera. Members of the group occupy diverse habitats and are distributed across the globe, though their greatest numbers and diversity are concentrated primarily in the tropics. Though continental endemism is common, many groups have a broad global distribution. An immense diversity of morphology is exhibited across the order with adult mantises ranging in size from 2cm to ~25cm, and appearing like a dead leaf, a piece of quartz rock, or a blade of grass. The diversification and specialization of mantises in ecologically diverse and biogeographically dispersed habitats suggest interesting questions about their morphological and behavioral adaptations. Despite their considerable popularity and consistent presence in the history of humanity, praying mantises have received surprising little attention from a phylogenetic or evolutionary standpoint. Though taxonomic studies have been thorough, discrepancies among classifications suggest wide latitude in the interpretation of morphological characters and their relative importance for grouping taxa. To address the lack of evolutionary knowledge surrounding praying mantises, the specific goals of this project were to: a) Reconstruct a comprehensive phylogeny for Mantodea using molecular characters; b) Use the phylogeny to elucidate character system evolution including hunting strategy, auditory evolution, and morphological convergences; and c) Investigate biogeographic patterns and determine the origins of the modern Mantodea. A comprehensive taxonomic and distributional sampling of Mantodea, covering virtually all higher-level groups, was assembled to reconstruct the phylogeny for the order. Sequence data were generated from five mitochondrial and four nuclear loci for 331 mantis species along with ten cockroach and termite species as outgroups. The resulting phylogenetic hypotheses served as the first glimpse of mantis evolutionary relationships and provided a template for further investigation. Only 7 of 15 families, 16 of 48 subfamilies, and 11 of 46 tribes were recovered as monophyletic indicating that phylogeny is largely incongruent with current mantis classification. As is the case in many other orders of insects, 'key characters' that do not reflect phylogeny are largely responsible for delimiting the groups. An investigation of mantis hunting strategy revealed clear transitions from generalist hunting mantises to the more derived strategies of cursorial and ambush hunting. In fact, the ambush hunting strategy appears to have evolved once, which led to a major diversification within the order. Some praying mantises have sensitive ultrasonic hearing arising from a unique 'cyclopean' ear located in the ventral metathorax. This project explored the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioral, and molecular databases. Using an 'auditory phylogeny' based on 13 morphological characters, a primitively earless form of metathoracic anatomy was indentified in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Mapping these results onto a phylogenetic tree derived from molecular data, shows that the cyclopean mantis ear evolved once 85-90 mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multi-component, in-flight behavior triggered by ultrasound. Thus, mantises have an ancient, highly conserved auditory neural-behavioral system that probably arose for evasion of echolocating predators. Modern bat families diverged ca. 63 mya, but the echolocating ancestors of bats appeared earlier. Alternatively, non-bat predators may have driven the evolution of the unique mantis auditory systems. Mapping biogeographic regions on the phylogeny demonstrated that our results adhere closer to geographic distribution than to the current classification. Specific patterns in distribution suggest that major morphological convergences have confounded taxonomists ability to construct natural groups. It was found that major mantis lineages diverged prior to the isolation of geographic regions and subsequent ecomorphic specializations within these regions led to convergences in morphology. Divergence time estimations place the origins of Mantodea at the beginning of the Jurassic with modern mantises originating on Gondwanaland in the Early Cretaceous. The first major divergence among modern mantises occurred as a result of the splitting of South America from Africa. The subsequent breakup of Gondwanaland continents spurred numerous divergences within the order and led to the contemporary paraphyletic assemblages of taxa within each biogeographic region. In fact, most divergences between Afrotropical and Indomalayan lineages resulted from the slow dissociation between Africa and the Indian subcontinent. Our results also suggest that Antarctica played an important role as a biological conduit during the diversification of some Afrotropical and Indomalayan lineages. Further, Antarctica facilitated the repeated invasions of South America and Australia prior to the separation of these two continents from Antarctica during the Eocene. When India slammed into Asia around 50 million years ago, it released a flood of mantises into Asia and Southeast Asia that diversified and currently comprise the largest component of Indomalayan taxa. The origins, secondary invasions, and regional extinctions have created an order of insects with complex distributional and evolutionary histories. |
author |
Svenson, Gavin John |
author_facet |
Svenson, Gavin John |
author_sort |
Svenson, Gavin John |
title |
The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
title_short |
The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
title_full |
The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
title_fullStr |
The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
title_full_unstemmed |
The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) |
title_sort |
origins, evolution, and phylogeny of the praying mantises (dictyoptera: mantodea) |
publisher |
BYU ScholarsArchive |
publishDate |
2007 |
url |
https://scholarsarchive.byu.edu/etd/1021 https://scholarsarchive.byu.edu/cgi/viewcontent.cgi?article=2020&context=etd |
work_keys_str_mv |
AT svensongavinjohn theoriginsevolutionandphylogenyoftheprayingmantisesdictyopteramantodea AT svensongavinjohn originsevolutionandphylogenyoftheprayingmantisesdictyopteramantodea |
_version_ |
1719473172953169920 |
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ndltd-BGMYU2-oai-scholarsarchive.byu.edu-etd-20202021-09-01T05:01:14Z The Origins, Evolution, and Phylogeny of the Praying Mantises (Dictyoptera: Mantodea) Svenson, Gavin John The relatively small insect order Mantodea (praying mantises) is comprised of approximately 2,366 described species distributed in 436 genera. Members of the group occupy diverse habitats and are distributed across the globe, though their greatest numbers and diversity are concentrated primarily in the tropics. Though continental endemism is common, many groups have a broad global distribution. An immense diversity of morphology is exhibited across the order with adult mantises ranging in size from 2cm to ~25cm, and appearing like a dead leaf, a piece of quartz rock, or a blade of grass. The diversification and specialization of mantises in ecologically diverse and biogeographically dispersed habitats suggest interesting questions about their morphological and behavioral adaptations. Despite their considerable popularity and consistent presence in the history of humanity, praying mantises have received surprising little attention from a phylogenetic or evolutionary standpoint. Though taxonomic studies have been thorough, discrepancies among classifications suggest wide latitude in the interpretation of morphological characters and their relative importance for grouping taxa. To address the lack of evolutionary knowledge surrounding praying mantises, the specific goals of this project were to: a) Reconstruct a comprehensive phylogeny for Mantodea using molecular characters; b) Use the phylogeny to elucidate character system evolution including hunting strategy, auditory evolution, and morphological convergences; and c) Investigate biogeographic patterns and determine the origins of the modern Mantodea. A comprehensive taxonomic and distributional sampling of Mantodea, covering virtually all higher-level groups, was assembled to reconstruct the phylogeny for the order. Sequence data were generated from five mitochondrial and four nuclear loci for 331 mantis species along with ten cockroach and termite species as outgroups. The resulting phylogenetic hypotheses served as the first glimpse of mantis evolutionary relationships and provided a template for further investigation. Only 7 of 15 families, 16 of 48 subfamilies, and 11 of 46 tribes were recovered as monophyletic indicating that phylogeny is largely incongruent with current mantis classification. As is the case in many other orders of insects, 'key characters' that do not reflect phylogeny are largely responsible for delimiting the groups. An investigation of mantis hunting strategy revealed clear transitions from generalist hunting mantises to the more derived strategies of cursorial and ambush hunting. In fact, the ambush hunting strategy appears to have evolved once, which led to a major diversification within the order. Some praying mantises have sensitive ultrasonic hearing arising from a unique 'cyclopean' ear located in the ventral metathorax. This project explored the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioral, and molecular databases. Using an 'auditory phylogeny' based on 13 morphological characters, a primitively earless form of metathoracic anatomy was indentified in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Mapping these results onto a phylogenetic tree derived from molecular data, shows that the cyclopean mantis ear evolved once 85-90 mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multi-component, in-flight behavior triggered by ultrasound. Thus, mantises have an ancient, highly conserved auditory neural-behavioral system that probably arose for evasion of echolocating predators. Modern bat families diverged ca. 63 mya, but the echolocating ancestors of bats appeared earlier. Alternatively, non-bat predators may have driven the evolution of the unique mantis auditory systems. Mapping biogeographic regions on the phylogeny demonstrated that our results adhere closer to geographic distribution than to the current classification. Specific patterns in distribution suggest that major morphological convergences have confounded taxonomists ability to construct natural groups. It was found that major mantis lineages diverged prior to the isolation of geographic regions and subsequent ecomorphic specializations within these regions led to convergences in morphology. Divergence time estimations place the origins of Mantodea at the beginning of the Jurassic with modern mantises originating on Gondwanaland in the Early Cretaceous. The first major divergence among modern mantises occurred as a result of the splitting of South America from Africa. The subsequent breakup of Gondwanaland continents spurred numerous divergences within the order and led to the contemporary paraphyletic assemblages of taxa within each biogeographic region. In fact, most divergences between Afrotropical and Indomalayan lineages resulted from the slow dissociation between Africa and the Indian subcontinent. Our results also suggest that Antarctica played an important role as a biological conduit during the diversification of some Afrotropical and Indomalayan lineages. Further, Antarctica facilitated the repeated invasions of South America and Australia prior to the separation of these two continents from Antarctica during the Eocene. When India slammed into Asia around 50 million years ago, it released a flood of mantises into Asia and Southeast Asia that diversified and currently comprise the largest component of Indomalayan taxa. The origins, secondary invasions, and regional extinctions have created an order of insects with complex distributional and evolutionary histories. 2007-07-16T07:00:00Z text application/pdf https://scholarsarchive.byu.edu/etd/1021 https://scholarsarchive.byu.edu/cgi/viewcontent.cgi?article=2020&context=etd http://lib.byu.edu/about/copyright/ Theses and Dissertations BYU ScholarsArchive Dictyoptera Mantodea Biogeography Systematics mantis praying mantis Auditory evolution Insect Biology |