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Genetic diversity and evolutionary age of parthenogenetic oribatid mites (Acari: Oribatida)

Heethoff, Michael (2004)
Genetic diversity and evolutionary age of parthenogenetic oribatid mites (Acari: Oribatida).
Technische Universität Darmstadt
Dissertation, Erstveröffentlichung

Kurzbeschreibung (Abstract)

Theories on the evolution and maintenance of sex are challenged by the existence of ancient asexual lineages like bdelloid rotifers and darwinulid ostracods. Ancient asexual origin of several speciose taxa has also been proposed for oribatid mites (Acari). In the present work, I analysed genetic divergences in different parthenogenetic and sexual lineages of oribatid mites to estimate the age of these lineages and to evaluate if the evolution of oribatid mites was without recombination. Age estimations were based on genetic distances of the mitochondrial gene for cytochrome oxidase I (COI) between clonal lineages of different parthenogenetic oribatid mite species. Species from two parthenogenetic taxa (Platynothrus peltifer, P. yamasakii, P. sibiricus, Heminothrus thori and Camisia horrida (Camisiidae) and Mucronothrus nasalis (Trhypochthoniidae)) were sampled in different sites in Europe, North America, South America, Australia and Asia. Corrected distances reached up to 157% on DNA level and 10% on amino acid level. Using different calibrations for a molecular clock, an age of up to 240 million years since the separation of the lineages was estimated. With this age, oribatid mites contain the oldest living parthenogenetic metazoan taxa. Further analyses investigated if the high evolutionary age of Platynothrus and other oribatid mite taxa (Mucronothrus nasalis, Tectocepheus velatus, Atropacarus striculus, Steganacarus magnus and Metabelba pulverulenta) was attained without gene recombination. To address this question, the two alleles of the hsp82 gene (coding for the 82 KD heat shock protein) were analysed for their genetic divergence. Due to gene recombination, sexual species in general have maximum divergences of 4% for this gene; higher amounts of divergence indicate absence of gene recombination as expected for parthenogenetic organisms. Genetic distances were up to 70% on DNA level and 15% on amino acid level indicating ancient lack of recombination. The absence of recombination in hsp82 was estimated to have happened 350 million years ago. The amount of genetic divergences between the alleles was in the same range in sexual and asexual oribatid mite species. High allelic divergence between hsp82 alleles in sexual and asexual species may be explained by the special mechanism of inheritance in oribatid mites: chromosomes are holokinetic and inverted meiosis has been inferred. If inverted meiosis occurs together with chiasma terminalisation gene recombination is suppressed in both sexual and parthenogenetic species. Together with terminal fusion in parthenogenetic species this mechanism resembles mitotic cloning. Inverted meiosis is a simple form of meiosis and it is discussed if this mechanism might be ancestral to “normal” meiosis. A scenario is proposed on how “normal” meiosis and monocentric chromosomes evolved from inverted meiosis and holokinetic chromosomes. Particular conditions may favour the frequent independent evolution and persistence of parthenogenetic clusters in oribatid mites. The absence of gene recombination in sexual and asexual oribatid mite species for at least 350 million years and the evolution of perhaps 100,000 oribatid mite species without gene recombination is an evolutionary mystery contradicting theories on sex and recombination and is unique in the animal kingdom.

Typ des Eintrags: Dissertation
Erschienen: 2004
Autor(en): Heethoff, Michael
Art des Eintrags: Erstveröffentlichung
Titel: Genetic diversity and evolutionary age of parthenogenetic oribatid mites (Acari: Oribatida)
Sprache: Englisch
Referenten: Norton, Prof. Dr. Roy A. ; Göringer, Prof. Dr. H. Ulrich
Berater: Scheu, Prof. Dr. Stefan
Publikationsjahr: 2 Februar 2004
Ort: Darmstadt
Verlag: Technische Universität
Datum der mündlichen Prüfung: 16 Dezember 2003
URL / URN: urn:nbn:de:tuda-tuprints-4011
Kurzbeschreibung (Abstract):

Theories on the evolution and maintenance of sex are challenged by the existence of ancient asexual lineages like bdelloid rotifers and darwinulid ostracods. Ancient asexual origin of several speciose taxa has also been proposed for oribatid mites (Acari). In the present work, I analysed genetic divergences in different parthenogenetic and sexual lineages of oribatid mites to estimate the age of these lineages and to evaluate if the evolution of oribatid mites was without recombination. Age estimations were based on genetic distances of the mitochondrial gene for cytochrome oxidase I (COI) between clonal lineages of different parthenogenetic oribatid mite species. Species from two parthenogenetic taxa (Platynothrus peltifer, P. yamasakii, P. sibiricus, Heminothrus thori and Camisia horrida (Camisiidae) and Mucronothrus nasalis (Trhypochthoniidae)) were sampled in different sites in Europe, North America, South America, Australia and Asia. Corrected distances reached up to 157% on DNA level and 10% on amino acid level. Using different calibrations for a molecular clock, an age of up to 240 million years since the separation of the lineages was estimated. With this age, oribatid mites contain the oldest living parthenogenetic metazoan taxa. Further analyses investigated if the high evolutionary age of Platynothrus and other oribatid mite taxa (Mucronothrus nasalis, Tectocepheus velatus, Atropacarus striculus, Steganacarus magnus and Metabelba pulverulenta) was attained without gene recombination. To address this question, the two alleles of the hsp82 gene (coding for the 82 KD heat shock protein) were analysed for their genetic divergence. Due to gene recombination, sexual species in general have maximum divergences of 4% for this gene; higher amounts of divergence indicate absence of gene recombination as expected for parthenogenetic organisms. Genetic distances were up to 70% on DNA level and 15% on amino acid level indicating ancient lack of recombination. The absence of recombination in hsp82 was estimated to have happened 350 million years ago. The amount of genetic divergences between the alleles was in the same range in sexual and asexual oribatid mite species. High allelic divergence between hsp82 alleles in sexual and asexual species may be explained by the special mechanism of inheritance in oribatid mites: chromosomes are holokinetic and inverted meiosis has been inferred. If inverted meiosis occurs together with chiasma terminalisation gene recombination is suppressed in both sexual and parthenogenetic species. Together with terminal fusion in parthenogenetic species this mechanism resembles mitotic cloning. Inverted meiosis is a simple form of meiosis and it is discussed if this mechanism might be ancestral to “normal” meiosis. A scenario is proposed on how “normal” meiosis and monocentric chromosomes evolved from inverted meiosis and holokinetic chromosomes. Particular conditions may favour the frequent independent evolution and persistence of parthenogenetic clusters in oribatid mites. The absence of gene recombination in sexual and asexual oribatid mite species for at least 350 million years and the evolution of perhaps 100,000 oribatid mite species without gene recombination is an evolutionary mystery contradicting theories on sex and recombination and is unique in the animal kingdom.

Alternatives oder übersetztes Abstract:
Alternatives AbstractSprache

Evolutionär alte parthenogenetische Linien wie die Bdelloidea (Rotifera) und die Darwinulidae (Ostracoda) sprechen gegen die Erwartungen von Evolutionstheorien zur sexuellen Reproduktion. Auch für einige Hornmilben-Arten wird angenommen, dass diese sich über evolutionäre Zeiträume ohne sexuelle Vorgänge fortpflanzen. In der vorliegenden Arbeit untersuchte ich die genetische Divergenz bei verschiedenen sexuellen und parthenogenetischen Hornmilben-Arten um das Alter dieser Linien zu bestimmen und um zu ermitteln, ob innerhalb der Linien genetische Rekombination stattfindet. Die Altersbestimmungen wurden über genetische Distanzen des mitochondriellen Gens für Cytochrom Oxidase I (COI) zwischen klonalen Linien verschiedener parthenogenetischer Arten vorgenommen. Es wurden mehrere Arten zweier parthenogenetischer Cluster untersucht (Platynothrus peltifer, P. yamasakii, P. sibiricus, Heminothrus thori und Camisia horrida (Camisiidae) und Mucronothrus nasalis (Trhypochthoniidae)). Diese wurden an verschiedenen Standorten in Europa, Nordamerika, Südamerika, Australien und Asien gesammelt. Die korrigierten Distanzen erreichten Werte von 157% bei den Nukleinsäuren und 10% bei den korrespondierenden Aminosäuren. Unter Berücksichtigung verschiedener Kalibrierungen für eine molekulare Uhr konnte ein evolutionäres Alter von bis zu 240 Millionen Jahre seit der Trennung der genetischen Linien berechnet werden. Damit wären einige parthenogenetische Hornmilben-Arten unter den ältesten eingeschlechtlichen Mehrzellern. In weiteren Untersuchungen sollte herausgefunden werden, ob dieses hohe evolutionäre Alter sexueller und parthenogenetischer Hornmilben (Mucronothrus nasalis, Tectocepheus velatus, Atropacarus striculus, Steganacarus magnus and Metabelba pulverulenta) ohne Rekombination erreicht wurde. Dazu wurde die Divergenz von den beiden Allelen des Gens für das 82 kD Hitzeschockprotein untersucht. Durch genetische Rekombination zeigen sexuelle Arten maximale allelische Divergenzen von etwa 4%; höhere Divergenzen deuten darauf hin, dass keine Rekombination stattfindet. Die allelischen Distanzen betrugen bis zu 70% auf DNA-Ebene und 15% im Protein, was auf langfristige Abwesenheit von Rekombination hindeutet. Rekombination könnte damit vor etwa 350 Millionen Jahren bei Hornmilben eingestellt worden sein. Die allelische Divergenz war bei sexuellen und parthenogenetischen Hornmilben in der gleichen Größenordnung. Dies kann durch den speziellen Reproduktionsmechanismus von Hornmilben erklärt werden: holokinetische Chromosomen und invertierte Meiose. Wenn invertierte Meiose zusammen mit Chiasmaterminalisierung auftritt, ist Rekombination funktioneller Gene weder bei sexuellen noch bei parthenogenetischen Arten möglich. Zusammen mit terminaler Fusion bei den parthenogenetischen Arten entspricht dieser Mechanismus mitotischem Keimbahnwachstum. Invertierte Meiose ist eine einfache Form der Meiose. Es ist unklar, welcher der beiden Mechanismen der ursprüngliche ist. Ich stelle ein mögliches Szenario vor, wie "normale" Meiose mit monozentrischen Chromosomen aus invertierter Meiose mit holokinetischen Chromosomen entstanden sein könnte.

Deutsch
Sachgruppe der Dewey Dezimalklassifikatin (DDC): 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften, Biologie
Fachbereich(e)/-gebiet(e): 10 Fachbereich Biologie
Hinterlegungsdatum: 17 Okt 2008 09:21
Letzte Änderung: 26 Aug 2018 21:24
PPN:
Referenten: Norton, Prof. Dr. Roy A. ; Göringer, Prof. Dr. H. Ulrich
Datum der mündlichen Prüfung / Verteidigung / mdl. Prüfung: 16 Dezember 2003
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