Amphibia-Reptilia 40 (2019): 121-127 brill.com/amre Short Note Phylogeographic evidence for multiple long-distance introductions of the common wall lizard associated with human trade and transport Joana L. Santos1, Anamarija Žagar1,2,3,∗, Katarina Drašler3, Catarina Rato1, César Ayres4, D. James Harris1, Miguel A. Carretero1, Daniele Salvi1,5,* Abstract. The common wall lizard has been widely introduced across Europe and overseas. We investigated the origin of putatively introduced Podarcis muralis populations from two southern Europe localities: (i) Ljubljana (Slovenia), where uncommon phenotypes were observed near the railway tracks and (ii) the port of Vigo (Spain), where the species was recently found 150 km far from its previously known range. We compared cytochrome-b mtDNA sequences of lizards from these populations with published sequences across the native range. Our results support the allochthonous status and multiple, long-distance origins in both populations. In Ljubljana, results support two different origins, Serbia and Italy. In Vigo, at least two separate origins are inferred, from western and eastern France. Such results confirm that human-mediated transport is promoting biological invasion and lineage admixture in this species. Solid knowledge of the origin and invasion pathways, as well as population monitoring, is crucial for management strategies to be successful. Keywords: biological invasions, human-mediated introduction, Podarcis muralis, population admixture, Slovenia, Spain. Introduction al., 2013). Species are transported to new lo- cations by different means, the importance of Biological invasions are one of the main threats which varies taxonomically, geographically and to biodiversity and together with habitat de- temporally. Often such introductions pose a risk struction and fragmentation are considered the to native biota, via processes such as competi- main causes behind recent biodiversity loss tive exclusion of native populations of ecolog- (Lee, 2002; Schulte et al., 2012; Simberloff et ically similar species, predation of native taxa, or through the possibility of invaders carry- ing diseases (Simberloff et al., 2013; Sacks et 1 - CIBIO Research Centre in Biodiversity and Genetic al., 2011). Consequently, this can lead to a de- Resources, InBIO, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, N° 7, 4485-661 crease of population size and fitness, promot- Vairão, Vila do Conde, Portugal ing partial isolation and strong selective pres- 2 - National insitute of Biology, Vecnaˇ pot 111, 1000 sure, compromising the continuity and stability Ljubljana, Slovenia of native populations (e.g. Sacks et al., 2011; 3 - Herpetological society – Societas herpetological Schulte et al., 2012). One particular problem slovenica, Vecnaˇ pot 111, 1000 Ljubljana, Slovenia 4 - Asociación Herpetológica Española, Museo Nacional is when populations of closely related species de Ciencias Naturales, C/ José Gutiérrez Abascal 2, or evolutionary lineages are introduced in the 28006 Madrid, Spain range of another, since they can compete with 5 - Department of Health, Life and Environmental Sci- native populations or interfere with reproduc- ences, University of L’Aquila, Via Vetoio, 67100 tion, resulting in hybridization (Allendorf et Coppito, L’Aquila, Italy ∗Corresponding authors; al. 2001; Lee, 2002; Schulte et al., 2012). In e-mails: [email protected]; fact, admixture between multiple conspecific [email protected] lineages, introduced into the same locality, can © Koninklijke Brill NV, Leiden, 2018. DOI:10.1163/15685381-20181040 122 J.L. Santos et al. increase genetic diversity and thus the invasive- This species is also widely introduced outside ness potential of a given species (Wagner et of its native range in Europe and North Amer- al., 2017). A remarkable number of cases of ica (Brown et al., 1995; Schulte et al., 2008; biological invasion in terrestrial habitats corre- Michaelides et al., 2013, 2015). While many spond to reptiles (with over 4500 introductions studies have assessed the origin and paths of reported since 1850; Kraus, 2009). The overall introductions in northern and central European frequency of species introductions is increasing, populations using molecular data (e.g. Schulte and lizards are not exceptions (e.g. Michaelides et al., 2015). Therefore, understanding the ori- et al., 2008, 2012; Michaelides et al., 2013, gin and pathways of introductions is essential 2015), to date little is known in the rest of the to corroborate the alien status of putative intro- species range duced populations, as well as to design effective We used mitochondrial cytochrome-b (cytb) management strategies to control or prevent in- DNA sequence data to assess the alien sta- vasions. tus and phylogeographic origin of two possi- The common wall lizard, Podarcis muralis bly introduced populations in urban and heavily (Laurenti, 1768) has the largest distribution humanized landscapes: (i) one from Ljubljana range among species of the genus Podarcis (Slovenia), where lizards showing uncommon (Wagler, 1830), including most of central Eu- phenotypes in terms of colouration were re- rope, Mediterranean peninsulas (Iberia, Italia, ported; and (ii) the second in Vigo (Spain), Balkans), and NW Anatolia (Sillero et al., 2014). Across this range, up to 23 evolution- which is outside the known species’ range. By ary lineages were identified, likely originat- comparing our new DNA sequences with those ing from multiple glacial refugia within the from native populations, we aimed to assess three Mediterranean peninsulas, but also in ex- their origin and, in case of introduction, to in- tra Mediterranean regions (Salvi et al., 2013). fer their possible pathway. Figure 1. (a) Maps of sampling locations for the two study-cases and representation of the distribution range of Podarcis muralis. (b) Satellite images with sampling localities and photographs of the habitat type for the two study-cases: Ljubljana, Slovenia and (c) port of Vigo, Spain. New introduced populations of Podarcis muralis 123 Materials and methods a morphological pattern distinct from native P. bocagei,also present in the area. Namely, P. muralis lizards from Vigo Two independent samplings were conducted in this study. In showed dark flanks contrasting with the dorsum, and bluish July 2013, nine samples were collected in Ljubljana (Slove- ocelli surrounded by dark colour on the shoulder, dark spots nia), in two different places separated by 1.5 km, across arranged in rows on the submaxilar scales and reddish or transects of approximately 200 m, next to the railway tracks white belly. (Location A1: Lat. 46.059°N, Lon. 14.504°E; Location A2: DNA extraction was performed using a high-saline Lat. 46.049°N, Lon. 14.491°E; fig. 1a, b). Podarcis muralis method (Sambrook et al., 1989) from tail tip tissues. The mi- is relatively common and widespread in Ljubljana (Krofel tochondrial cytb gene was amplified by Polymerase Chain et al., 2009), with a typical mostly uniformly brown dor- Reaction using the primers CytbG and cb2R (Palumbi et al., sal colouration, and a red or white ventral colouration in 1991). The amplified cytb fragment overlaps with the frag- both males and females. However, the observed sampled in- ment sequenced by Salvi et al. (2013). Amplification con- dividuals had uncommonly interconnected dark patches and ditions were as in Mendes et al. (2017) and sequencing re- a light greenish colouration on the dorsal side, with an or- actions were conducted by an external company, Genewiz ange or white ventral colouration. (UK). In September 2017, four samples of P. muralis were col- Electropherograms were checked and consensus se- lected at the maritime port of Vigo (NW Spain), along the quences were aligned using MUSCLE implemented in Bouzas seafront near a carpark for cargo boats (Location Geneious v4.8.5 (Biomatters Ltd). The dataset includes nine B1: Lat. 42.232°N, Lon. −8.761W; fig. 1a, c). This popu- sequences of P. muralis from Ljubljana and four from Vigo, lation was found 150 km to the west of the closest previ- generated in this study, and 185 sequences downloaded ously known population, and outside of the range predicted from GenBank used in Salvi et al. (2013). Podarcis liolepis by ecological models (Cabana et al., 2016). A tissue sample (GenBank accession number KF372218) was designated as from the tail and photographs were collected for each indi- an outgroup. Phylogenetic relationships were inferred us- vidual. The sampled lizards were easily identified, showing ing the Maximum Likelihood (ML) method implemented Figure 2. (a) Maximum likelihood phylogenetic tree based on 198 cytb mtDNA sequences of Podarcis muralis sampled for this study and across its native range. Bootstrap values over 1,000 replicates are reported in correspondence of the nodes; nodes with a support lower than 30% were collapsed. The mitochondrial clades are numbered from 1 to 23, according to Salvi et al. (2013). The clades including the 13 new samples from Ljubljana (highlighted in pink) and Vigo (highlighted in cyan) are expanded in the boxes with detailed information on geographic origin of sequenced individuals (SRB: Serbia; SL: Slovenia; KR: Croatia; ITA: Italy; AUS: Austria; FR: France; ES: Spain; Andorra: Andorra; GER: Germany). (b) Map with the putative distribution range of P. muralis lineages (modified from Salvi et al., 2013); grey shade: native range; dots: introduced populations known in Germany and Great Britain; arrows: lineages
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