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Mitochondrial DNA Control Region Diversity in Common Terns Sterna

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Mitochondrial DNA Control Region Diversity in Common Terns Sterna Acrocephalus 40 (180/181): 69–78, 2019 10.1515/acro-2019-0004 Mitochondrial DNA control region diversity in Common Terns Sterna hirundo from Slovenia and Croatia Raznolikost kontrolne regije mitohondrijske DNK pri navadni čigri Sterna hirundo iz Slovenije in Hrvaške Ida Svetličić1, Jelena Kralj2, Miloš Martinović2, Davorin Tome 3, Tilen Basle4, Luka Božić4, Iztok Škornik5, Luka Jurinović6, Ana Galov1* 1 University of Zagreb, Faculty of Science, Department of Biology, Rooseveltov trg 6, Zagreb, Croatia, e-mail: [email protected], [email protected] 2 Institute of Ornithology, Croatian Academy of Sciences and Arts, Gundulićeva 24, Zagreb, Croatia, e-mail: [email protected], [email protected] 3 National Institute of Biology, Večna pot 111, Ljubljana, Slovenia, e-mail: [email protected] 4 DOPPS – BirdLife Slovenia, Tržaška cesta 2, Ljubljana, Slovenia, e-mail: [email protected], [email protected] 5 Sečovlje Salina Nature Park, SOLINE Pridelava Soli d.o.o., Seča 115, Portorož, Slovenia, e-mail: [email protected] 6 Croatian Veterinary Institute, Poultry Centre, Heinzelova 55, Zagreb, Croatia, e-mail: [email protected] * corresponding author 63 Common Tern Sterna hirundo samples from Croatia and Slovenia were analysed with respect to their genetic diversity and differentiation. Samples originated from two freshwater populations (areas of the rivers Sava and Drava) and one coastal population (Sečovlje Salina). The molecular marker of choice was 709 bp long fragment of the mitochondrial control region, the fastest-evolving part of the mitochondrial genome. 21 haplotypes with 12 polymorphic sites were identified. Overall haplotype diversity was substantial and estimated at 0.8599, while the overall nucleotide diversity was low and estimated at 0.0025. Diversity indices were highest for the Drava population, followed by the Sava and the lowest for the Sečovlje population. Overall genetic structure was significantly low (Fst=0.0377) and attributed to the differences in haplotype frequencies between the populations. The high level of genetic diversity found in continental populations illustrates the importance of their habitats as reservoirs of genetic diversity and calls for their further protection and management. Key words: mtDNA, freshwater colonies, population genetics, Laridae, seabird Ključne besede: mtDNA, celinske kolonije, populacijska genetika, Laridae, morske ptice 1. Introduction and subarctic regions of Europe, Asia and North America. It is a long-distance migrator, winter- Common Tern Sterna hirundo is a coloni- ing in tropical and subtropical coastal regions. al seabird of the family Laridae that breeds both Despite being listed as a species of least concern on freshwater and marine habitats of temperate by the IUCN, the global population trend is 69 I. Svetličić et al.: Mitochondrial DNA control region diversity in Common Terns Sterna hirundo from Slovenia and Croatia mostly unknown on account of variation in ty of the mitochondrial DNA (mtDNA) control trends between different populations Birdlife( region genetic analysis is its exceptionally high International 2018). Freshwater colonies are polymorphism coupled with conserved arrange- located mostly on river and lake islands. They are ment of neighbour genes, which allows for con- under a strong negative influence of anthropo- sistent amplification by polymerase chain reaction genic activities, mainly river regulation, as well as with many primers. Extreme polymorphism aids under natural threats (e.g. competition with gulls in identification of interpopulation as well as in- and mammalian predation), which has led to a sig- trapopulation lineages. Furthermore, an important nificant global reduction of the natural freshwa- property of mtDNA is the uniparental inheritance ter breeding sites. Freshwater populations of the which results in a lack of recombination. Individ- Common Tern are now almost entirely dependent ual lineages can thus be traced through time in a on artificial sites, specifically rafts and gravel islands more straightforward manner than with nuclear (Becker & Ludwigs 2004). Freshwater breeding markers. Moreover, mtDNA is more sensitive to de- sites in Slovenia and Croatia can be found along mographic changes such as bottlenecks and popula- the river Sava where the most important breeding tion expansion due to its haploid nature (Freeland site is Rakitje (Martinović et al. 2019) and in et al. 2011). Despite downsides to mtDNA analyses the river Drava area where the main colony inhab- (Hurst & Jiggins 2005), mitochondrial DNA has its the Ptuj reservoir. Many small coastal colonies remained the marker of choice in many population are located along the Adriatic Sea, while one of the and phylogeographic studies. largest is located in Sečovlje Salina Nature Park in One of the first population genetic studies of the Northern Adriatic (Denac et al. 2019). Common Terns was undertaken on populations Despite ongoing research, dynamics of both from North America, using isoelectric focusing of freshwater and coastal populations in Croatia and blood proteins. High levels of gene flow were sug- Slovenia are still relatively unclear. High breed- gested among four colonies as no genetic differen- ing site fidelity, a well-known characteristic of the tiation was found (Burson III 1990). It was fol- Common Tern (Austin 1949) and many other lowed by an investigation of Lithuanian colonies seabird species (Palestis 2014, Coulson 2016), using allozymes where some genetic differentiation can favour population differentiation by restricting was reported (Sruoga et al. 2002). Further in- gene flow Friesen( et al. 2007). Therefore, popu- vestigations were performed using nuclear genetic lation substructuring in long-distance migratory markers, specifically microsatellite loci, where sig- seabirds is seemingly driven by behaviour rather nificant differentiation among sampled locations than by physical land barriers (Friesen et al. 2007, was found in Lithuania (Sruoga et al. 2006) and Szczys et al. 2017A). in the North Atlantic region (Szczys et al. 2012). Genetic studies on wild animal populations are A later study by Szczys et al. (2017B) on cy- mostly performed using neutral genetic markers such tochrome B revealed hierarchical metapopulation as mitochondrial DNA control region and microsat- structure with the presence of small- and large-scale ellites, which are suitable for studies of genetic diver- connectivity between metapopulations. sity, genetic structure and demographic processes of To our knowledge, there are no published pop- populations. Genetic diversity estimation constitutes ulation genetic studies of Common Tern inferred the basis of many contemporary conservation efforts from an analysis of the mitochondrial DNA control because it is crucial for the evolutionary potential region marker. Thus, in this paper we provide the of species and therefore one of the keys for its long- first assessment of mtDNA control region diversi- term survival (Van Dyke 2008). It can thus serve as a ty of Common Terns in general. The goal of this measure of the species capacity for future adaptation study was to analyse a 709 bp long fragment of the to environmental challenges. mitochondrial control region in two continental, The control region is the fastest evolving part freshwater populations of Common Terns from of the mitochondrial genome, traditionally used Slovenia and Croatia and in a coastal population as a marker in population genetic and phylogeo- from Slovenia (Sečovlje Salina). Considering the graphic studies. One of the reasons for the ubiqui- local and global threats affecting freshwater tern 70 Acrocephalus 40 (180/181): 69–78, 2019 habitats, this study aimed to quantify the levels of determine the number of haplotypes (H), assign genetic diversity in populations of Common Terns haplotypes to the individuals, determine the number from the three geographic areas as well as to detect of variable positions, nucleotide composition, and a possible phylogeographic structure. Furthermore, for calculation of haplotype diversity (Hd) – the the intention was to gain insight into possible ex- probability that two randomly chosen sequences are pansions or bottlenecks in their population history. different. The mean number of pairwise differences and nucleotide diversity (π) – the probability that 2. Methods the two homologous nucleotides differentiate – were calculated with Arlequin as well. AMOVA (Analysis We caught 63 Common Terns during their of Molecular Variance) was conducted in order to breeding period in the spring and summer of 2017 investigate spatial genetic structuring by analyzing (6 individuals), 2018 (54 individuals) and 2019 covariance components utilizing information on (3 individuals). Sampling took place in gravel pits haplotype frequencies and nucleotide distance near the river Sava (30 individuals), the river Drava between haplotypes (Excoffier et al. 1992), as (22 individuals from Ptuj accumulation and 2 implemented in Arlequin. Population groups were individuals further downstream) and in Sečovlje defined as ‘’Sava’’, ‘’Drava’’ and ‘’Sečovlje’’. Pairwise Salina (9 individuals) (Figure 1). Around 50 µL of FST and ΦST values for each group were calculated blood was taken from the brachial vein and stored in Arlequin as well. Significance was tested using either in EDTA coated tubes on ice or on bloodstain 10,000 non-parametric permutation procedures. storage cards (Nucleocard, Machery Nagel), while DnaSp (Rozas et al. 2017) was
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