Can Novel Genetic Analyses Help to Identify Lowdispersal Marine
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Can novel genetic analyses help to identify low-dispersal marine invasive species? Peter R. Teske1,2, Jonathan Sandoval-Castillo1, Jonathan M. Waters3 & Luciano B. Beheregaray1 1Molecular Ecology Laboratory, School of Biological Sciences, Flinders University, Adelaide, South Australia 5001, Australia 2Department of Zoology, University of Johannesburg, Auckland Park, 2006, Johannesburg, South Africa 3Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand Keywords Abstract Ascidian, biological invasion, coalescent theory, founder effect, genetic bottleneck, Genetic methods can be a powerful tool to resolve the native versus introduced microsatellites, sea squirt. status of populations whose taxonomy and biogeography are poorly understood. The genetic study of introduced species is presently dominated by analyses that Correspondence identify signatures of recent colonization by means of summary statistics. Unfor- Luciano B. Beheregaray tunately, such approaches cannot be used in low-dispersal species, in which Molecular Ecology Laboratory, School of recently established populations originating from elsewhere in the species’ native Biological Sciences, Flinders University, range also experience periods of low population size because they are founded by Adelaide, SA 5001, Australia. Tel: +61 8 8201 5243; Fax: +61 8 8201 3015; few individuals. We tested whether coalescent-based molecular analyses that pro- E-mail: Luciano.beheregaray@flinders.edu.au vide detailed information about demographic history supported the hypothesis that a sea squirt whose distribution is centered on Tasmania was recently intro- Funding Information duced to mainland Australia and New Zealand through human activities. Meth- This study was funded by the Australian ods comparing trends in population size (Bayesian Skyline Plots and Research Council (DP110101275 to Approximate Bayesian Computation) were no more informative than summary Beheregaray, Moller€ & Waters). statistics, likely because of recent intra-Tasmanian dispersal. However, IMa2 esti- Received: 19 April 2014; Revised: 4 May mates of divergence between putatively native and introduced populations pro- 2014; Accepted: 6 May 2014 vided information at a temporal scale suitable to differentiate between recent (potentially anthropogenic) introductions and ancient divergence, and indicated Ecology and Evolution 2014; 4(14): 2848– that all three non-Tasmanian populations were founded during the period of 2866 European settlement. While this approach can be affected by inaccurate molecular dating, it has considerable (albeit largely unexplored) potential to corroborate doi: 10.1002/ece3.1129 nongenetic information in species with limited dispersal capabilities. Introduction human-introduced species that were previously unable to establish large populations (Diederich et al. 2005; Thuiller Marine biological invasions pose considerable evolution- et al. 2007) but also by driving poleward range shifts in ary, ecological, and economic consequences (Grosholz numerous regions (Ling 2008; Pitt et al. 2010), making it 2002; Bax et al. 2003; Molnar et al. 2008). Even though ever more difficult to distinguish between natural and the problem is well recognized, the number of non-native anthropogenic introductions. species arriving in new habitats as a consequence of The early detection of non-indigenous species increases human activities such as shipping and aquaculture opera- the chances of eradicating them before they can fully tions continues unabatedly (Molnar et al. 2008; Occhipin- establish themselves (Bax et al. 2001; Lodge et al. 2006), ti-Ambrogi and Galil 2010). This not only increases the but it is often difficult to distinguish between native and chances of potential invaders establishing themselves but recently established populations of marine species because also increases the risk of intraspecific hybridization of the lack of systematic, biogeographic, and historical among successively introduced propagules from different data (Carlton 2009). Such uncertainty can present major localities in the species’ native range, which can increase challenges for managers who must prioritize management invasive success because the increased genetic variation of unwanted species. makes adaptive evolution more likely (Ellstrand and Schi- In marine ecosystems, populations of introduced erenbeck 2000). Global climate change exacerbates this species can sometimes be characterized by their ecologi- trend, not only by facilitating the invasion of habitats by cal association with disturbed or artificial habitats 2848 ª 2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. P. R. Teske et al. Genetic Identification of Low-Dispersal Aliens (particularly in harbors, which present the most likely marine species is native or introduced (e.g., Turon et al. points of introduction; Carlton and Geller 1993) and by 2003; Xavier et al. 2009; Stefaniak et al. 2012). This situa- life histories that are conducive to dispersal by means of tion is clearly very different from what has been reported anthropogenic vectors (e.g., attachment to ships’ hulls, or for species with high dispersal potential. The latter often transport in ballast water; Lacoursiere-Roussel et al. show low levels of genetic structure and similar levels of 2012). However, it is often difficult to rule out the alter- diversity along their native ranges (Kyle and Boulding native explanation that populations in question represent 2000; Banks et al. 2007) and also between source regions previously overlooked native taxa (e.g., Teske et al. and areas into which they have recently extended their 2011a). In such cases, genetic information is often consid- ranges (e.g., Hassan and Bonhomme 2005; Banks et al. ered a particularly powerful means of conclusively identi- 2010). fying a non-native organism. The study of known or putatively introduced species The most frequently applied criteria for identifying has until recently been dominated by various approaches introduced species include (a) large geographic distances of measuring genetic diversity, and tests that determine between the ranges of potentially introduced populations whether or not a bottleneck has occurred, without pro- and their closest relatives (i.e., their likely source popula- viding information on its magnitude and duration. tions; Carlton and Geller 1993), which is particularly The fact that the loss of genetic diversity during an compelling in the case of trans-oceanic invasions (Geller introduction is often limited or even absent, particularly et al. 2010); and (b) relatively low genetic diversities in when the bottleneck was brief and subsequent population non-native versus native populations, reflecting founder expansion rapid (Carson 1990), or when multiple intro- effects in the former (Roman and Darling 2007). Unfor- ductions occurred (Roman 2006), clearly highlights the tunately, there are many examples in which neither of limitations of such methods. During the past decade, a these two criteria can be used to reliably diagnose inva- suite of more sophisticated approaches has been devel- sions. First, many introductions do not involve interoce- oped that can be used to reconstruct demographic histo- anic transport, but meso-scale colonization events (often ries in considerable detail. Most of these are Bayesian following a stepping-stone pattern) into habitats that a methods based on coalescent theory (Kingman 1982), and particular species can theoretically reach without an programs in which they are implemented include IMa2 anthropogenic vector (Hassan et al. 2003; Golani et al. (Hey 2010), DIYABC (Cornuet et al. 2014) and BEAST 2007). Second, genetic diversity indices of recently estab- (Drummond et al. 2012). Although none of these novel lished populations can be comparatively high when these methods were developed to specifically distinguish originated from multiple, genetically differentiated sources between native and introduced populations, their utility (Roman 2006), although this is readily recognizable when in answering questions about periods of population these are represented by genetically distinct lineages decline and expansion, and divergence between popula- (Perez-Portela et al. 2013). Third, in taxa that lack a tions, suggests that they have great potential in uncover- long-lived dispersal phase, it is difficult to distinguish ing demographic information that can help to inform between natural and recently established populations on management decisions. the basis of genetic diversity even when the latter origi- The necessity of identifying new genetic approaches nated from a single source. Recruitment in these low-dis- that can contribute toward resolving the native versus persal species is predominantly local such that each site in introduced status of low-dispersal species is illustrated by the native range has a unique combination of alleles (Tes- a survey of the recent literature of genetic studies on ke et al. 2011b), and dispersal over greater distances is ascidians (Urochordata, Tunicata, Ascidiacea) (Table 1), often only possible by means of rafting (e.g., association a group of sessile marine invertebrates that includes a with floating objects such as wood or seaweed; Thiel and number of important invasive species (Lambert 2007). Gutow