Aspects of the molecular ecology of Bombus (Hymenoptera: Apidae) in Europe
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1 Research Collection Doctoral Thesis Aspects of the molecular ecology of Bombus (Hymenoptera: Apidae) in Europe Author(s): Widmer, Alexander Publication Date: 1996 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETHNr ASPECTS OF THE MOLECULAR ECOLOGY OF BOMBUS (HYMENOPTERA: APIDAE) IN EUROPE A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH presented by Alexander Widmer dipl.natw.eth born March 9, 1969 citizen of Basel (BS) and Herrenhof (TG) Accepted on the recommendation of: Prof.Dr.P.Schmid-Hempel (examiner) Prof.Dr.P.Pamilo (co-examiner) Prof.Dr.M.Wolfe (co-examiner) 1996
3 2 SUMMARY 1. Bumble bees (Hymenoptera: Apidae: Bombus spp.) are primitively eusocial insects with an annual life cycle. In central and northern Europe, the colony cycle starts after hibernation of the mated queens, whereas queens in southern Europe and on Mediterranean islands aestivate. The colony may consist of several worker generations. Males and young queens are produced towards the end of the colony cycle. Soon after mating, young queens retreat into their hibernation or aestivation places, while the rest of the colony dies. To what extent young queens and males disperse from their native population is unknown. The exchange of individuals and genes between populations affects genetic diversity and population structure. We used molecular markers to estimate genetic diversity in bumble bees and to obtain indirect estimates of gene flow and population differentiation. 2. Genetic variability at allozyme loci has been found to be low in Hymenoptera before. A new analysis of allozyme variation in 248 insect species revealed that haplodiploidy per se does not significantly reduce genetic variability and that eusociality has no consistent effect on allozyme variation between Hymenoptera of different degrees of eusociality. While primitively eusocial wasps were found to be slightly more variable than solitary ones, the opposite tendency was observed in bees. A preliminary analysis of heterozygosity at microsatellite loci further suggested that low allozyme variability in Hymenoptera is not a genome-wide phenomenon but rather an oddity of allozymes. The Hymenoptera were found to be as variable at microsatellite loci as the Diptera. However, further data are needed to assess the reliability of this observation. 3. Because genetic variation at allozyme loci is generally low in Hymenoptera and in particular in Bombus. microsatellites were used as nuclear genetic markers throughout this study. Extensive genetic variation is the result of high mutation rates in the number of simple sequence repeats. These markers were used in combination with mitochondrial DNA sequence data to assess genetic population structure and phylogeography in Bombus terrestris and Bombus pascuorum. 4. Populations of Bombus terrestris from the Canary Islands, Madeira and Mediterranean islands are genetically differentiated from each other and from continental populations. Microsatellite polymorphisms revealed that genetic variability within island populations is reduced with respect to continental populations. Mitochondrial DNA sequence data provided information about the phylogeographic history of the insular and continental
4 3 populations and revealed that the mtdna haplotypes from the Canary Islands and from the Tyrrhenian Islands are restricted to these islands. A comparison with B.lucorum further revealed that these haplotypes are plesiomorphic with respect to the haplotypes found on the European continent. These results suggest a long history of B.terrestris on the Canary Islands and the Tyrrhenian Islands, which probably were colonized prior to the last glacial period in Europe. The absence of primitive mtdna haplotypes and the lack of genetic differentiation among continental populations may be evidence for the occurrence of one or repeated bottlenecks during the last ice age and a rapid subsequent range expansion. 5. While no evidence for isolation by distance was observed among continental populations of Bombus terrestris. increasing distance of islands from the continent led to enhanced differentiation. The effect of distance on gene flow and thus on differentiation, however, varied between groups of islands. Historical processes, such as the colonization history of these islands, may be responsible for the observed differences. 6. Significant genetic differentiation was found among several continental populations of the bumble bee Bombus pascuorum. Within geographic regions and in the absence of barriers, such as mountains, gene flow among neighbouring populations was found to be intense and consequently genetic differentiation was low or absent. On the other hand, strong differentiation between populations north and south of the Alps revealed that the Alps represent an effective barrier to gene flow in this species. However, gene flow over the Alps can occur sometimes, such as over the Reschenpass IAUJ. As a consequence, a contact zone between the northern subspecies B.p.floralis and the southern subspecies B.p.pascuorum exists in this area. Indirect evidence for the existence of this contact zone came from the observation of a northern mtdna haplotype in the population Latsch that is located south of the Alps. Patterns of genetic variation at nuclear and mitochondrial loci, assessed by microsatellite and mtdna sequence polymorphisms, respectively, were in good agreement and supported the division of the populations in a northern and a southern gene pool with limited genetic exchange. 7. A molecular study of the European members of the subgenus Bombus Latreille sensu stricto based on mtdna sequence data supported the recognition of four genetically distinct taxa in Europe. The morphological similarity of the species is in contrast to the considerable genetic divergence. A reliable assessment of the phylogenetic relationships among the species was not possible. Phylogenetic trees reconstructed from partial COII and 16s rrna sequence data, respectively, led to different hypotheses about the evolutionary relationships among the species. This result stresses the necessary
5 4 distinction between gene trees and organismal trees and emphasizes the need for phylogenetic studies that are based on several unlinked loci. 8. This study revealed that Bombus spp. are genetically variable, in contrast to electrophoretic evidence from allozymes. Microsatellites were found to be reliable markers for the study of genetic variability and population differentiation in bumble bees. Despite their high mutation rate, the intraspecific phylogenetic relationships deduced from these nuclear markers were generally in good agreement with mtdna sequence information. ZUSAMMENFASSUNG 1. Hummeln (Hymenoptera: Apidae: Bombus spp.) sind primitiv eusoziale Insekten mit einem einjahrigen Lebenszyklus. In Zentral- und Nordeuropa beginnt der Koloniezyklus nachdem die begatteten Koniginnen ihren Winterschlaf beendet haben; die Koniginnen in Siideuropa und auf den Inseln im Mittelmeer legen eine Sommerruhe ein. In einem Nest konnen mehrere Generationen von Arbeiterinnen gebildet werden. Gegen Ende des Koloniezyklus schlupfen die Mannchen und die jungen Koniginnen. Bald nach der Kopulation ziehen sich die Jungkoniginnen in ihre Uberwinterungs-, resp. Ubersommerungsverstecke zuriick, wahrend der Rest der Kolonie stirbt. Es ist nicht bekannt wie weit sich die Jungkoniginnen und Mannchen von ihren Geburtspopulationen entfernen. Der Austausch von Individuen und Genen zwischen Populationen hat einen Einfluss auf die genetische Variabilitat und bestimmt die Populationsstruktur. Um eine indirekte Schatzung fiir den Genfluss und die Differenzierung zwischen Populationen, sowie fiir das Ausmass an genetischer Vielfalt zu erhalten, haben wir molekulargenetische Marker verwendet. 2. Bereits friiher wurde festgestellt, dass Hymenopteren iiber eine geringe Allozymvariabilitat verfugen. Eine neue Analyse der genetischen Vielfalt an Allozymloci von 248 Insektenarten hat ergeben, dass Haplodiploidie alleine nicht zu einem signifikantem Verlust an genetischer Vielfalt fiihrt. Im weiteren hat Eusozialitat keinen gleichmassigen Einfluss auf die Diversitatsunterschiede zwischen Hymenopteren mit unterschiedlich entwickelter Eusozialitat. Wahrend primitiv eusoziale Wespen ein hoheres Mass an Variabilitat aufweisen als solitare Wespen, fand sich bei Bienen ein
6 5 gegensatzlicher Trend. Eine vorlaufige Analyse der Heterozygositatswerte an Mikrosatellitenloci hat im weiteren die Vermutung nahe gelegt, dass die geringe Allozymvariabilitat der Hymenopteren kein Phanomen darstellt, welches fiir das Gesamtgenom reprasentativ ist, sondern vielmehr eine Eigenheit der Allozyme ist. Die Hymenopteren wiesen im Vergleich mit den Dipteren keine reduzierte Mikrosatellitenvariabilitat auf. Weitere Daten sind jedoch notwendig, Beobachtung zu stutzen oder zu verwerfen. um diese 3. Da die Allozymvariabilitat der Hymenopteren, und insbesondere der Vertreter der Gattung Bombus. generell genetische genetischer tief ist, haben wir in dieser Arbeit Mikrosatelliten als Marker fur die Variabilitat der Zellkern-DNA verwendet. Das hohe Masss an Vielfalt ist das Resultat hoher Mutationsraten an Mikrosatellitenloci. Diese genetischen Marker wurden gemeinsam mit DNA-Sequenzen Genoms dazu verwendet, die genetische Verwandtschaftsbeziehungen von Populationen Populationsstruktur des mitochondrialen und die historischen innerhalb der beiden Hummelarten Bombus terrestris (Dunkle Erdhummel) und Bombus pascuorum (Ackerhummel) zu studieren. 4. Populationen von Bombus terrestris. die von den Kanarischen Inseln, Madeira und einigen Mittelmeerinseln stammen, sind genetisch differenziert voneinander und auch von Festlandpopulationen. Inselpopulationen sind im Vergleich mit Festlandpopulationen genetisch verarmt, wie Mikrosatellitenuntersuchungen ergeben haben. DNA-Sequenzen des mitochondrialen Genoms ergaben Hinweise auf historische Verwandtschaftsbeziehungen zwischen Insel- und Festlandpopulationen und zeigten auf, dass die mitochondrialen Haplotypen, welche auf den Kanarischen und den Tyrrhenischen Inseln gefunden wurden, nur dort vorkommen. Ein Vergleich mit B.lucorum (Helle Erdhummel) ergab im weiteren, dass diese Haplotypen urspriinglicher sind als jene, die auf dem Europaischen Festland gefunden wurden. Diese Resultate legen den Schluss nahe, dass B.terrestris die Kanarischen und Tyrrhenischen Inseln seit langer Zeit bewohnt und diese wahrscheinlich bereits vor der letzten Eiszeit besiedelt hat. Die Abwesenheit primitiver mitochondrialer Haplotypen und das Fehlen genetischer Differenzierung zwischen kontinentalen Populationen konnte ein Hinweis fiir das Auftreten eines oder mehrerer Populationsengpasse wahrend der letzten Eiszeit und einer raschen anschliessenden Wiederbesiedlung sein. 5. Wahrend wir bei kontinentalen Populationen keine Hinweise fiir einen signifikanten Zusammenhang zwischen genetischer Differenzierung und geographischer Distanz gefunden haben, hat bei Inselpopulationen eine zunehmende Distanz vom Festland zu erhohter Differenzierung gefuhrt. Zwischen verschiedenen Inselgruppen fanden sich
7 jedoch 6 Unterschiede im Einfluss der Distanz vom Festland auf den Genfluss, und somit auch auf die Differenzierung. Historische Prozesse, wie die Besiedlungsgeschichte dieser Inseln, konnten fur die gefundenen Unterschiede verantwortlich sein. 6. Wir fanden, dass einige Populationen der Hummelart Bombus pascuorum signifikant von einander differenziert sind. Innerhalb geographischer Regionen und in Abwesenheit von Hindernissen, wie Bergen, fand reger Genfluss zwischen benachbarten Populationen statt, weshalb kaum oder keine Differenzierung auftrat. Andererseits wies starke genetische Differenzierung zwischen Populationen nordlich und siidlich der Alpen darauf hin, dass die Alpen den Genfluss innerhalb dieser Art stark einschranken. Trotzdem kann Genfluss iiber die Alpen stattfinden, wie zum Beispiel am Reschenpass [AU]. Als Folge davon hat sich eine Kontaktzone zwischen der nordlichen Unterart B.p.pfloralis und der siidlichen Unterart B.p.pascuorum gebildet. Einen indirekten Hinweis dafiir fand sich darin, dass wir in Latsch, also siidlich der Alpen, einen mitochondrialen Haplotypen fanden, der typisch fur Populationen nordlicher der Alpen ist. Die Verteilung genetischer Vielfalt bei den nuklearen Loci und einem mitochondrialen Locus stimmten weitgehend iiberein und unterstiitzten die Unterteilung der Populationen in einen nordlichen und einen siidlichen Genpool mit geringem genetischem Austausch. 7. Eine molekulare Untersuchung der europaischen Arten der Untergattung Bombus Latreille im engeren Sinne, die auf mitochondrialen DNA-Sequenzen basierte, unterstiitzte die Anerkennung vier genetisch unterscheidbarer Taxa in Europa. Die morphologische Ahnlichkeit der Arten steht im Kontrast zur deutlichen genetischen Differenzierung. Es war uns nicht moglich, die Verwandtschaftsbeziehungen zwischen den Arten zu klaren. Phylogenetische Stammbaume, die basierend auf Sequenzen der Cytochrom Oxidase- Untereinheit II und der 16s rrna erstellt wurden, legten unterschiedliche Verwandtschaftsbeziehungen nahe. Diese Resultate weisen nachdriicklich darauf hin, dass Stammbaume einzelner Gene nicht notwendigerweise mit den Stammbaumen der untersuchten Organismen iibereinstimmen. Es ist deshalb unumganglich, dass Untersuchungen von Verwandtschaftsbeziehungen auf mehreren, voneinander unabhangigen, Genloci basieren. 8. Diese Studie hat gezeigt, dass Arten der Gattung Bombus genetische Variabilitat aufweisen, was im Gegensatz zu Resultaten aus Untersuchungen steht, die sich auf Allozyme beschrankt haben. Wir fanden, dass Mikrosatelliten zuverlassige Marker fiir die Untersuchung genetischer Vielfalt und Populationsdifferenzierung bei Hummeln sind. Trotz der hohen Mutationsrate von Mikrosatelliten stimmten die innerartlichen Verwandtschaftsbeziehungen, welche basierend auf diesen Daten erhoben wurden, weitgehend mit jenen iiberein, welche basierend auf mitochondrialer DNA erstellt wurden.
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