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Evolutionary Ecology of Cryptic Amphipod Species

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Evolutionary Ecology of Cryptic Amphipod Species Eawag_06569 DISS. ETH NO. 19650 Evolutionary ecology of cryptic amphipod species A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences presented by ANJA MARIE WESTRAM MSc, University of Münster June 22, 1983 citizen of Germany accepted on the recommendation of Prof. Dr. Jukka Jokela Prof. Dr. Roger K. Butlin 2011 Table of contents 1‐4 Summary / Zusammenfassung 5‐12 General introduction 13‐32 Chapter I: Spatial distribution of cryptic species diversity in European freshwater amphipods as revealed by pyrosequencing 33‐38 Chapter II: Isolation and characterization of ten polymorphic microsatellite markers for three cryptic Gammarus fossarum (Amphipoda) species 39‐62 Chapter III: Hidden biodiversity in a freshwater keystone species ‐ Population genetic analysis reveals substantial biological and historical differences between two cryptic amphipod spe‐ cies 63‐84 Chapter IV: Are cryptic host species also cryptic to parasites? Host specificity and geographi‐ cal distribution of acanthocephalan parasites infecting freshwater Gammarus 85‐90 Concluding remarks 91‐94 Acknowledgements 95‐96 Curriculum Vitae Summary / Zusammenfassung Summary Cryptic species are morphologically very similar, but reproductively isolated and sometimes evolu‐ tionarily old. They might differ in any trait other than morphology, including ecological, behavioural and physiological characteristics. If we do not recognize cryptic species and their biological differ‐ ences, biodiversity assessments, functional ecosystem studies, and conservation measures might be inadequate. Studies that identify cryptic species and the differences between them are therefore urgently needed especially for endangered taxa and ecological keystone taxa. In my doctoral thesis, I studied cryptic species of the ecologically important freshwater amphipod Gammarus fossarum. This morphospecies is an important fish prey, shredder of organic material, and host for parasites, therefore playing a key role in stream ecosystems. Previous studies have shown that G. fossarum contains at least three morphologically cryptic species, types A, B, and C. I focused on differences between these species with regard to geographical distribution, population genetic structure (which reflects biological characteristics and historical processes), and interactions with parasites. In chapter I, I describe the geographical distribution of the three cryptic species in Central Europe. I use a novel pyrosequencing assay for rapid species identification of samples from Switzerland, and combine these data with results from previous studies to find a clear geographical distribution pat‐ tern: While type C is rare and occurs only in a few populations in the west of the studied area, type A is common in the east and type B in the west. A contact zone located in the Rhine drainage connects the distribution ranges of type A and type B. This distribution is consistent with recolonization from distinct glacial refugia after the Pleistocene glaciations. The description of the contact zone will be valuable for future studies as it indicates the area where several species co‐occur and studies on G. fossarum will require species identification based on molecular markers. In chapters II and III, I use populations characterized in chapter I for detailed population genetic stud‐ ies. The degree and spatial distribution of genetic structure are indicative of biological traits (e.g., dispersal abilities) as well as historical processes. Using microsatellite markers developed for all cryp‐ tic species in chapter II, I find large differences between type A and B (chapter III): While genetic structure is associated with geography in both species, the extent of genetic differentiation between populations is much higher in type A than in type B. This result strongly suggests that the two species will differ markedly in their reactions to environmental stress and threats of local extinction. More‐ over, the genetic patterns suggest a recent spread of type B into the Rhine drainage. Type A, which shows evidence of long‐term persistence in the Rhine drainage, might currently be displaced by type B. 2 Chapter IV focuses on the interaction between the cryptic G. fossarum species with acanthocephalan parasites. After sampling infected G. fossarum from multiple populations, I identify parasite species using a molecular marker. I find that several species of Acanthocephala known to usually infect G. pulex (a more distantly related Gammarus species) also successfully infect G. fossarum. The two most common parasite species are able to infect both type A and B, corroborating the hypothesis that these parasites have broad host ranges. However, infections are generally less common in type A, suggesting different coevolutionary histories of the two cryptic species. My PhD thesis demonstrates differences between two cryptic species in all three aspects under study (geographical distribution, population genetic structure, and interactions with parasites). Type A and B most likely differ in their reactions to environmental changes as well as in their role in the ecosys‐ tem. This study therefore underlines the importance of considering cryptic species as separate enti‐ ties in basic and applied research. Zusammenfassung Kryptische Arten sind reproduktiv isoliert, jedoch morphologisch sehr ähnlich. In allen nicht‐morphologischen Merkmalen, z.B. ihrer Ökologie, ihrer Physiologie und ihrem Verhalten, können sie sich dennoch deutlich unter‐ scheiden. Werden kryptische Arten in Studien zur Biodiversität oder zu funktionalen Zusammenhängen in Öko‐ systemen nicht berücksichtigt, kann dies zu grossen Ungenauigkeiten führen, die einen wirkungsvollen Natur‐ schutz erschweren. Forschungsprojekte zur Identifizierung kryptischer Arten und der Unterschiede zwischen ihnen sind somit unerlässlich, vor allem wenn es um bedrohte Arten oder Schlüsselarten in Ökosystemen geht. In meiner Doktorarbeit habe ich kryptische Arten des Gammarus fossarum‐Artkomplexes untersucht, der wich‐ tige ökologische Funktionen im Bachökosystem erfüllt. G. fossarum dient als Hauptnahrungsquelle für viele Fischarten, ist Zerkleinerer von totem organischem Material und dient als Zwischenwirt für unterschiedliche Parasiten. Frühere Arbeiten haben gezeigt, dass G. fossarum aus mindestens drei kryptischen Arten besteht, die als Typ A, B und C bezeichnet werden. Ich habe mich hier auf die Unterschiede zwischen diesen Arten in Bezug auf ihre geographische Verteilung, ihre populationsgenetische Struktur (die biologische Eigenschaften und historische Prozesse widerspiegelt) und ihre Interaktionen mit Parasiten konzentriert. In Kapitel I beschreibe ich die geographische Verteilung der drei kryptischen Arten. Die Ergebnisse der Artbe‐ stimmung von Gammaridenpopulationen aus der Schweiz mithilfe eines neuartigen Pyrosequencing‐Protokolls ergeben kombiniert mit Resultaten früherer Studien ein klares Bild der Verteilung in Mitteleuropa: Während Typ C selten ist und nur in einigen wenigen Populationen im Westen des Untersuchungsgebietes vorkommt, ist Typ A im Osten häufig und Typ B im Westen. Eine Kontaktzone innerhalb des Rhein‐Einzugsgebietes verbindet die Verbreitungsgebiete von Typ A und B. Die beobachtete Verteilung stimmt mit der Hypothese überein, dass Typ A und Typ B Mitteleuropa nach der letzten Eiszeit aus unterschiedlichen Refugien wiederbesiedelt haben. 3 Meine Arbeit identifiziert das Gebiet, in dem Typ A und B gemeinsam vorkommen und wo für zukünftige wis‐ senschaftliche Studien somit jeweils eine molekulare Artbestimmung erforderlich ist. In den Kapiteln II und III untersuche ich einige der in Kapitel I identifizierten Populationen genauer in Bezug auf ihre populationsgenetische Struktur. Das Ausmass sowie das räumliche Muster genetischer Unterschiede liefert Hinweise auf biologische Merkmale (z.B. Verbreitungsfähigkeiten) und historische Prozesse. Mithilfe neu ent‐ wickelter Mikrosatellitenmarker (Kapitel II) zeige ich deutliche Unterschiede zwischen Typ A und Typ B (Kapitel III): Während in beiden Arten die populationsgenetische Struktur von der Geographie geprägt ist, ist das Aus‐ mass der genetischen Differenzierung in Typ A deutlich höher als in Typ B. Dieses Resultat zeigt, dass die beiden Arten höchstwahrscheinlich sehr unterschiedlich reagieren, wenn sich ihre Umwelt verändert oder sie lokal vom Aussterben bedroht sind. Die genetischen Daten liefern zusätzliche Hinweise darauf, dass sich Typ B erst kürzlich im Rhein‐Einzugsgebiet ausgebreitet hat, während die Typ A‐Populationen schon länger etabliert sind. Kapitel IV befasst sich mit der Interaktion zwischen G. fossarum und Parasiten vom Stamm der Acanthocepha‐ la. Parasiten aus zahlreichen G. fossarum‐Populationen wurden mithilfe molekularer Marker bestimmt. Ich konnte zeigen, dass mehrere Parasitenarten, von denen allgemein bekannt war, dass sie G. pulex (eine weitere in der Schweiz vorkommende Gammarus‐Art) infizieren, auch G. fossarum befallen können. Die beiden am häufigsten gefundenen Parasitenarten können sowohl Typ A als auch Typ B infizieren, was die Annahme bestä‐ tigt, dass diese Parasiten generell ein breites Wirtsspektrum haben. Infektionen waren jedoch in Typ A generell seltener, was auf unterschiedliche koevolutionäre Prozesse in der Vergangenheit der beiden kryptischen Arten hinweist. Meine Arbeit zeigt deutliche Unterschiede zwischen zwei morphologisch nicht unterscheidbaren Arten in allen untersuchten Aspekten (geographische Verbreitung, populationsgenetische Struktur, und Wirt‐Parasit‐
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