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Population Genetics of the Invasive Cryptogenic Anemone, Anemonia Alicemartinae, Along the Southeastern Pacific Coast

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Population Genetics of the Invasive Cryptogenic Anemone, Anemonia Alicemartinae, Along the Southeastern Pacific Coast Journal of Sea Research 102 (2015) 1–9 Contents lists available at ScienceDirect Journal of Sea Research journal homepage: www.elsevier.com/locate/seares Population genetics of the invasive cryptogenic anemone, Anemonia alicemartinae, along the southeastern Pacific coast C.B. Canales-Aguirre a,b,c,A.Quiñonesa,C.E.Hernándezb,P.E.Neilla,d, A. Brante a,⁎ a Departamento de Ecología. Facultad de Ciencias. Universidad Católica de la Santísima Concepción, Casilla 294, Concepción, Chile b Laboratorio de Ecología Evolutiva y Filoinformática, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción Casilla 160-C, Concepción, Chile c Laboratorio de Genética y Acuicultura, Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción Casilla 160-C, Concepción, Chile d The Thomas Jefferson School, Department of Applied Sciences, Ave. Jorge Alessandri, Parcela 26, Concepción, Chile article info abstract Article history: One of the most important issues in biological invasions is understanding the factors and mechanisms determin- Received 5 March 2014 ing the invasion success of non-native species. Theoretical and empirical works have shown that genetic diversity Received in revised form 24 March 2015 is a determinant of invasion success; thus, studying spatial patterns of genetic diversity, and exploring how bio- Accepted 26 March 2015 logical and physical factors shape this population trait, are fundamental for understanding this phenomenon. Available online 3 April 2015 Coastal marine ecosystems are one of the most susceptible habitats to invasion given the complex network of maritime transport. In this work we study the cryptogenic anemone, Anemonia alicemartinae, which has rapidly Keywords: COI increased its geographical range southward during the last 50 years (approx. 2000 km) along the southeastern Demographic Expansion Pacific coast. Based on COI mtDNA sequences we evaluated three main hypotheses: a) the genetic diversity of Human-mediated Transport A. alicemartinae decreases according to the direction of invasion (from north to south); b) there is biogeographic– Humboldt Current Ecosystem phylogeographic concordance at the 30°S biogeographic break; and c) the demographic history is coherent with a Invasion Genetics recent geographic expansion. A total of 161 individual samples of A. alicemartinae were collected along the south- Marine Invasions eastern Pacific coast range of distribution, covering more than 2000 km, including samples along the 30°S biogeo- graphical break. Results showed low genetic diversity (Hd = 0.253; π = 0.08) and a lack of geographic population genetic structure (FST = −0.009, p-value = 0.656). The highest genetic diversity was observed in Peru (Chero and Mesas) and at localities close to the main Chilean seaports. We did not observe concordance be- tween biogeographic and phylogeographic patterns or isolation by distance. Demographic indices (D = −2.604, p b 0.001; Fu's = −26.619, p b 0.001), as well as a star-like configuration of the haplotype network support recent population expansion of this species. Our results, together with historical field observations, support the idea that the current distribution of A. alicemartinae may be explained by an increase in population size from one small ances- tral population probably from the south of Peru, with subsequent human-mediated southward transport, probably associated with regional-scale maritime activities. © 2015 Published by Elsevier B.V. 1. Introduction fundamental for understanding this phenomenon. Also, revealing the underlying factors of invasions may help managers to implement poli- Invasion biology seeks to identify the evolutionary mechanisms cies and mitigation actions. underlying the success of invasive species (Sakai et al., 2001). Genetic Theoretical models and experimental data have shown that small diversity is one of the main population traits determining the evolution- populations, which characterize the initial processes of invasion, are sub- ary and adaptive potential of a species to new habitat conditions (e.g. ject to the founder effect, dominated by low genetic diversity and strong Lavergne and Molofsky, 2007; Reed and Frankham, 2003; Tsutsui genetic drift (England et al., 2003; Leberg, 1992; McCommas and Bryant, et al., 2000). In this sense, studying geographic patterns of genetic diver- 1990; Nei et al., 1975). Genetic drift is expected to act strongly at the in- sity in an invasive species, and exploring how biological and physical vasion front, given the reduced size of the newly colonizing population. factors shape genetic diversity during the invasion process, are Once the invader population is established in the new habitat, a signa- ture of recent genetic expansion may be evident at the first stage of population spread (Sakai et al., 2001). In this way, assuming only one invasion event, three main expectations may arise: (1) populations of ⁎ Corresponding author. Tel.: +56 41 234 5642. invaders show chronic low genetic diversity, (2) genetic diversity de- E-mail addresses: [email protected] (C.B. Canales-Aguirre), [email protected] (A. Quiñones), [email protected] creases toward the front of the invasion, and (3) a signature of genetic (C.E. Hernández), [email protected] (P.E. Neill), [email protected] (A. Brante). expansion is observed in the invader population. http://dx.doi.org/10.1016/j.seares.2015.03.005 1385-1101/© 2015 Published by Elsevier B.V. 2 C.B. Canales-Aguirre et al. / Journal of Sea Research 102 (2015) 1–9 In addition to the demographic dynamic of invasions (e.g. the foun- reproduction may be an important reproductive strategy in populations der effect), the combination of abiotic local environmental characteris- of this species on the Chilean coast (Häussermann and Försterra, 2001). tics (e.g. current patterns, thermal gradients), as well as biological Currently, the distribution of A. alicemartinae covers over 2000 km of characteristics of the invader (e.g. reproductive strategies, dispersal ca- the Chilean coastline, from 17°S to 37°S, crossing a well-documented pacity) also shape the spatial distributional pattern of genetic diversity oceanographic break at 30°S (Hormazabal, 2004), which defines two (Chomsky et al., 2009; Severance and Karl, 2006; Sherman and Ayre, biogeographic provinces: the Peruvian Province and the Intermediate 2008; Sherman et al., 2007). In general, invasive species with high dis- Province (Camus, 2001). In addition, at an intraspecific level, this ocean- persal potential should have faster invasion rates and higher invasion ographic discontinuity affects the dispersal patterns of many marine in- success (Schreiber and Lloyd Smith, 2009), showing low or null popula- vertebrate species, including organisms with both, high and low tion genetic structure in the new habitat (Marrs et al., 2008; Roderick dispersal potentials, resulting in an important phylogeographic barrier and Navajas, 2003). In contrast, strong barriers for dispersal, such as nat- (e.g. Haye et al., 2014; Sánchez et al., 2011). No study has evaluated ural biogeographic barriers, would retard or stop the advance of the in- whether this strong environmental and ecological break at 30°S may vaders. In this case, when human-mediated transport is not involved in have some effect on A. alicemartinae ecology or on spatial patterns of the subsequent invasion process, the invasive species population should genetic diversity. present genetic structure concordant with the biogeographic– The purpose of this study is to describe the spatial pattern of phylogeographic break (Zardi et al., 2007). population genetic diversity in the cryptogenic anemone invader, Coastal marine ecosystems are one of the most susceptible habitats A. alicemartinae. Based on mitochondrial DNA (mtDNA) sequences, to invasion given the complex network of maritime transport (Kaluza we evaluated whether: a) the genetic diversity of A. alicemartinae et al., 2010; Molnar et al., 2008), which can override the effect of natural decreases according to the direction of invasion (from north to south); biogeographical barriers, sometimes resulting in the introduction of b) populations are genetically structured along the species' distribution small invading populations. Anemonia alicemartinae is an invasive cryp- or whether there is a consistency between biogeographic and phylogeo- togenic anemone on the Chilean coast, described in 2001, and character- graphic boundaries along the southeastern Pacific coast; and c) the ized by its deep red color, high population densities in intertidal and demographic history is coherent with a recent geographic expansion. shallow subtidal zones, and rapid geographic expansion southward along the southeastern Pacific coast (Häussermann and Försterra, 2. Materials and methods 2001). In early marine biodiversity records of the Chilean coast (i.e. 1959 to 1965) this species was absent; with the first record in northern 2.1. Sampling zone Chile (20°16′S, Iquique) in 1975 (see Castilla et al., 2005). During the 1980s, A. alicemartinae was reported further south, in Coquimbo A total of 161 individuals of A. alicemartinae were collected from the (30°S), in high abundances, but was absent at sites south of this point. shallow subtidal and rocky intertidal zone, at eight locations throughout Later, in 1998 a small population was recorded in central-southern its geographical distribution, covering a range of 2200 km of coastline, Chile at
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