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Genetic Diversity of the Stone Crayfish

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Genetic Diversity of the Stone Crayfish University of Zagreb Faculty of Science Lena Bonassin and Ljudevit Luka Boštjančić GENETIC DIVERSITY OF THE STONE CRAYFISH Zagreb, 2019. This research has been conducted in the Laboratory for molecular analyses, Division of Zoology, Department of Biology, Faculty of Science, University of Zagreb, under the guidance of Dr. Ivana Maguire, Prof. and Dr. Martina Podnar Lešić and submitted for the rector's award in the academic year 2018/2019. Ovaj rad izrađen je u Laboratoriju za molekularne analize Zoologijskog zavoda Biološkog odsjeka, Prirodoslovno-matematičkog fakulteta Sveučilišta u Zagrebu pod vodstvom prof. dr. sc. Ivane Maguire i dr. sc. Martine Podnar Lešić i predan je na natječaj za dodjelu Rektorove nagrade u akademskoj godini 2018./2019. Abbreviations 16S rRNA – 16S ribosomal RNA ABGD – Automatic Barcode Gap Discovery BA – Bayesian analysis BEAST – Bayesian Evolutionary Analysis Sampling Trees *BEAST – Star BEAST, Bayesian framework for species tree estimation BIC – Bayesian information criterion BIN – Barcode Index Number bp – base pair BPP – Bayesian posterior probability bPTP – Bayesian implementation of the Poisson Tree Processes (PTP) model for species delimitation COI – cytochrome c oxidase subunit I gene DnaSP – DNA Sequence Polymorphism ESS – Estimated Sample Size F – empirical base frequencies G – gamma distribution GMYC – Generalized Mixed Yule Coalescent (GMYC) method HKY – Hasegawa-Kishino-Yano evolution model HPD - highest posterior density I – invariant sites ITS2 – Internal Transcribed Spacer 2 IUCN – International Union for Conservation of Nature I JC – Jukes and Cantor evolution model Ka – thousand years ago K2P – Kimura 2-parameter K3Pu – three substitution types model and unequal base frequencies Ma – million years ago MAFFT – multiple sequence alignment based on fast Fourier transform ML – maximum likelihood MMCM – Metropolis-coupled Monte Carlo Markov chain MP – maximum parsimony NSV – node support value OTU – operational taxonomic unit PAUP – Phylogenetic Analysis Using Parsimony PAUP* – Phylogenetic Analysis Using PAUP PTP – Poisson Tree Processes subs/s/my/l – substitution per site per million years per lineage TBR – Tree-Bisection-Reconnection TCS – Templeton, Crandall and Sing method tcsBU – Templeton,Crandall and Sing (TCS) Beautifier II Contents Abbreviations .............................................................................................................................. I 1. Introduction ........................................................................................................................ 1 2. General and specific aims................................................................................................... 6 3. Methods .............................................................................................................................. 7 3.1. Sampling scheme ......................................................................................................... 7 3.2. DNA extraction, gene amplification and sequencing .................................................. 8 3.3. Sequence data .............................................................................................................. 9 3.4. Phylogenetic reconstruction......................................................................................... 9 3.4.1. Mitochondrial DNA ............................................................................................. 9 3.4.2. Nuclear DNA ...................................................................................................... 11 3.5. Genetic diversity and haplotype networks ................................................................. 11 3.6. Time of divergence .................................................................................................... 12 3.7. Species delimitation ................................................................................................... 13 3.8. Species validation ...................................................................................................... 14 4. Results .............................................................................................................................. 16 4.1. Sequence data ............................................................................................................ 16 Phylogenetic reconstruction ................................................................................................. 17 4.1.1. Mitochondrial DNA ........................................................................................... 17 4.1.2. Nuclear DNA ...................................................................................................... 19 4.2. Genetic diversity ........................................................................................................ 19 4.3. Population structure ................................................................................................... 23 4.4. Time of divergence .................................................................................................... 25 4.5. Species delimitation ................................................................................................... 28 4.6. Species validation ...................................................................................................... 33 5. Discussion ........................................................................................................................ 38 5.1. Evolutionary history .................................................................................................. 38 5.2. Phylogenetic structure ............................................................................................... 44 5.3. Species delimitation ................................................................................................... 48 5.4. Conservation .............................................................................................................. 50 6. Conclusion ........................................................................................................................ 51 7. Aknowledgments .............................................................................................................. 53 8. Bibliography ..................................................................................................................... 54 9. Appendix .......................................................................................................................... 70 10. Summary ....................................................................................................................... 83 11. Sažetak .......................................................................................................................... 84 12. Curriculum vitae ........................................................................................................... 85 1. Introduction The stone crayfish Austropotamobius torrentium (Schrank, 1803) (Figure 1) is the smallest of five European indigenous crayfish species and is considered a keystone species in freshwater ecosystems because of its role in preserving ecosystem stability and biodiversity (Füreder et al., 2006; Reynolds, 2006; Reynolds et al., 2013). It inhabits smaller streams and brooks at higher altitudes of central and south-eastern Europe (Holdich et al., 2006; Kouba et al, 2014; Maguire et al., 2018). The stone crayfish areal of distribution extends from Germany and the Czech Republic in the north, to Luxembourg in the west, to Greece in the south, and Turkey and Bulgaria in the east (Holdich et al., 2006). Although their endemic areal of distribution is limited, they possess high genetic diversity preserved in eight distinct mtDNA lineages separated by prominent genetic gaps (Trontelj et al., 2005; Klobučar et al., 2013; Pârvulescu et al., 2019). Figure 1. Stone crayfish Austropotamobius torrentium (Schrank, 1803) (Photographed by Nataša Pršir) In recent years many studies have shown that populations of A. torrentium, as well as other indigenous European crayfish species (Astacus astacus, Astacus leptodactylus, Astacus pachypus, Austropotamobius pallipes) are declining (Kouba et al., 2014; Maguire et al., 1 2018). They are threatened by both biotic and abiotic factors such as habitat deterioration (Holdich et al., 2009; Weinländer et al., 2014), water quality decline (Svobodová et al., 2017), climate changes (manifested as prolonged/extreme droughts) (Maguire et al., 2011; Kouba et al., 2016), the presence/spread of non-indigenous invasive American crayfish species and their pathogens (eg. Aphanomyces astaci, the causative agent of the crayfish plague, disease that is lethal for indigenous crayfish species) (Souty-Grosset, 2016; Maguire et al., 2016; Jussila et al., 2017). Since A. torrentium is considered to be the most sensitive species of indigenous European crayfishes, and it is particularly sensitive to warm and polluted waters (Repina Potočki, 2016), it is protected by both national (NN 80/13, NN 144/2013) and international laws and listed in the Annexes II and V of the EU Habitats Directive (Council directive 92/43/EEC, 2000). The conservation status of A. torrentium is not yet resolved in all European countries since it is classified as data deficient on the IUCN Red List (Füreder et al., 2010). In Croatia, as a result of the existence of historical and present data on the distribution and population size, the species is listed as vulnerable
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