Shifts in Morphology and Diet of Non-Native Sticklebacks Introduced

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Shifts in Morphology and Diet of Non-Native Sticklebacks Introduced Shifts in morphology and diet of non-native sticklebacks introduced into Japanese crater lakes Tatsuya Adachi1, Asano Ishikawa2, Seiichi Mori3, Wataru Makino1, Manabu Kume3, Masakado Kawata1 & Jun Kitano1,2,4 1Division of Ecology and Evolutionary Biology, Graduate School of Life Sciencefs, Tohoku University, Sendai, Miyagi 980-8578, Japan 2Ecological Genetics Laboratory, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan 3Biological Laboratory, Gifu-keizai University, Ogaki, Gifu 503-8550, Japan 4PRESTO, Japan Science and Technology Agency, Honcho Kawaguchi, Saitama 332-0012, Japan Keywords Abstract Adaptation, anthropogenic, caldera, contemporary evolution, fisheries, invasive, An increasing number of exotic animals are causing ecological problems. There- rapid evolution. fore, for better ecosystem management, it is important to understand how exotic Correspondence species colonize and adapt to novel environments. The threespine sticklebacks Jun Kitano, Ecological Genetics Laboratory, (Gasterosteus aculeatus) can be a good vertebrate model system to explore the eco- National Institute of Genetics, Yata 1111, logical and genetic mechanisms of adaptation not only in natural populations, but Mishima, Shizuoka 411-8540, Japan. Tel: also in non-native populations. Although morphological changes have been doc- 81-55-981-9415; Fax: 81-55-981-9416; umented in several introduced populations of stickleback, little is known about E-mail: [email protected] the dietary changes during colonization into novel environments. Here, we investi- This research is supported by JST PRESTO gated the morphological and dietary changes of exotic threespine stickleback pop- program, Asahi Glass Foundation, Grant-in-Aid ulations introduced into three Japanese crater lakes (Lake Towada, Lake Kussharo, for Young Scientist (B) (22770075) and and Lake Shikotsu). Sticklebacks were introduced into the crater lakes likely along Grant-in-Aid for Scientific Research on with salmonids transplanted for aquaculture. The stickleback population in Lake Innovative Areas (23113007 and 23113001) Kussharo had multiple mitochondrial haplotypes and had larger phenotypic vari- from the Ministry of Education, Science, ances than other crater lake stickleback populations that had only one mitochondrial Sports, and Culture to J. K. and NIG Collaborative Research Program (2011-A68, haplotype. Compilation of historical data on the morphology and stomach contents A69). A. I. is a fellow of the Japan Society of of the Lake Towada stickleback population showed that substantial shifts in body Promotion of Science. size and stomach contents occurred after colonization. Some of these changes may berelatedtoanoutbreakoftheSchistocephalus parasite. These results suggest that Received: 19 January 2012; Revised: 9 February 2012; Accepted: 13 February 2012 sticklebacks can change their morphology and trophic ecology when they colonize novel environments. Therefore, extreme care should be taken when salmonids are Ecology and Evolution 2012; 2(6): transported between watersheds for aquaculture and that long-term monitoring of 1083–1098 exotic species is essential for ecosystem management. In addition, further genetic studies on phenotypic changes in crater lake sticklebacks would help elucidate the doi: 10.1002/ece3.234 genetic mechanisms underlying the adaptation of exotic fishes to novel environ- ments. and sports, or unintentionally, such as when they contami- Introduction nate the transplanted stocks of other organisms (Jeschke and An increasing number of animals have been transplanted Strayer 2005, 2006). Meta-analyses of biological invasions from native habitats to novel environments (Elton 1958; have demonstrated that human affiliates, such as domesti- Sakai et al. 2001). Because exotic species are causing many cates, pets, human commensals, have high invasion success ecological problems, it is important to understand how (Jeschke and Strayer 2005, 2006) and the success rate of in- exotic species invade, colonize, and adapt to novel envi- vasion increases when humans intend their establishment ronments for better management of ecosystem functions (Ruesink 2005). Therefore, it is important to identify the (Pejchar and Mooney 2009). Exotic species have been inten- dispersal pathways of exotic species to prevent their further tionally introduced for specific reasons, such as aquaculture colonization. c 2012 The Authors. Published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 1083 Commons Attribution Non Commercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Crater Lake Sticklebacks T. Adachi et al. (Bell and Foster 1994; Schluter 2000; McKinnon and Rundle 2002). In addition, previous studies have characterized phe- notypic changes in exotic populations introduced into fresh- water ponds, lakes, and lagoons (Klepaker 1993; Kristjansson´ et al. 2002; Aguirre et al. 2004; Bell et al. 2004; Lucek et al. 2010). Although these studies have demonstrated substantial phenotypic changes in foraging traits, which might occur as adaptation to dietary shifts, they have not directly tested di- etary changes of the introduced populations. Furthermore, genetic structures of the introduced populations have not been investigated except in a case of a Swiss population (Lucek et al. 2010). The present study aimed to characterize phenotypic and dietary changes of exotic populations of threespine stickle- back that were introduced into three crater lakes. We also Figure 1. Threespine stickleback (Gasterosteus aculeatus) in a crater investigated genetic structures of the introduced crater lake lake, Lake Kussharo. populations. Crater lakes provide an interesting ecosystem for investigating the invasion by exotic species, because these lakes were formed by volcanoes, so they were originally de- Furthermore, the mechanisms through which exotic pauperate (Barluenga et al. 2006; Barluenga and Meyer 2010; species adapt to novel environments should be elucidated. Elmer et al. 2010). Depauperate environments with vacant There are several empirical examples of the introduced pop- niches often provide a stage for biological diversification and ulations changing their phenotypes after the colonization of have been extensively investigated in evolutionary ecology novel environments (Hendry and Kinnison 1999; Reznick (MacArthur and Wilson 1967; Diamond 1974; Whittaker and Ghalambor 2001; Bossdorf et al. 2005; Huey et al. 2005). and Fernandez-Palacios´ 2007). The colonization of organ- Such phenotypic changes can occur by both phenotypic plas- isms into crater lakes occurs through multiple routes, such ticity and genetic changes (Hendry et al. 2011). When ge- as immigration through newly formed rivers and introduc- netic changes are crucial, the genetic variances of introduced tion by hurricanes, animals, and human release (Hikita and populations can influence the success rate of colonization Taniguchi 1959; Tokui 1964; Ban and Suzuki 2003; Elmer et al. (Willi et al. 2006; Hendry et al. 2011). For example, multiple 2010). Thus, the investigation of nascent ecological commu- introductions or hybridizations between different popula- nities in crater lakes will provide a window into the early tions may increase genetic variances and promote adaptation stages of community assembly. Furthermore, the investiga- (Kolbe et al. 2004; Facon et al. 2005; Lockwood et al. 2007). tion of impacts of exotic species on the crater lake ecosystem In addition, even in cases where phenotypic plasticity plays is important for management of ecosystem services provided an important role in adaptation, increased genetic variances by crater lakes, because crater lakes are often used for aqua- may improve the plasticity of exotic species, because phe- culture and sightseeing and are important financial resources notypic plasticity is usually a heritable trait (De Jong 1990; for local communities (JFRCA 2004a, b). Scheiner 1993; Pigliucci 2005). Therefore, genetic studies of The threespine sticklebacks have been found in three crater introduced species and investigation of the genetic mecha- lakes in Japan (Fig. 2A; Table 1). The most plausible route of nisms of adaptation are crucial for better management of colonization into crater lakes is human release. Although exotic species (Hendry et al. 2011). no fish were found in Lake Towada during the 19th century The threespine sticklebacks (Gasterosteus aculeatus)can (Hikita and Taniguchi 1959; Tokui 1959), landlocked forms of be an excellent vertebrate model system to explore the eco- Oncorhynchus nerka (kokanee) have been stocked in the lake logical and genetic mechanisms of adaptation not only in nat- since the early 1900s. Several other exotic fishes, such as carp ural populations, but also in non-native populations (Fig. 1). (Cyprinus carpio), smelt (Hypomesus transpacificus nipponen- The ecological and genetic mechanisms underlying adaptive sis), masu salmon (Oncorhynchus masou), char (Salvenilus evolution during the last postglacial dispersal have been ex- leucomaenis), threespine stickleback, nine-spined stickleback tensively investigated in sticklebacks (Schluter 2000; Shapiro (Pungitius sinensis), and loach (Misgurnus anguillicaudatus) et al. 2004; Colosimo et al. 2005; Miller et al. 2007; Chan can be also found in Lake Towada today (JFRCA 2004b). Al- et al. 2010; Hohenlohe et al. 2010). Ancestral marine stick-
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