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Arctic Char (Salvelinus Alpinus) and Dolly Varden (Salvelinus Malma) Are Not Two Sides of the Same Coin

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Arctic Char (Salvelinus Alpinus) and Dolly Varden (Salvelinus Malma) Are Not Two Sides of the Same Coin doi:10.1111/j.1420-9101.2008.01603.x Genetic analysis of sympatric char populations in western Alaska: Arctic char (Salvelinus alpinus) and Dolly Varden (Salvelinus malma) are not two sides of the same coin E. B. TAYLOR,* E. LOWERY, A. LILLIESTRA˚ LE,*,à A. ELZ§ & T. P. QUINN *Department of Zoology, Biodiversity Research Centre and Native Fishes Research Group, University of British Columbia, Vancouver, BC, Canada School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA àUppsala University, Biology Education Center, Uppsala, Sweden §NOAA Fisheries Service, Northwest Fisheries Science Center, East Seattle, WA, USA Keywords: Abstract microsatellites; The North Pacific Ocean has been of great significance to understanding morphology; biogeography and speciation in temperate faunas, including for two species of mtDNA; char (Salmonidae: Salvelinus) whose evolutionary relationship has been reproductive isolation; controversial. We examined the morphology and genetics (microsatellite Salvelinus; and mitochondrial DNA) of Arctic char (Salvelinus alpinus) and Dolly Varden sympatric populations. char (Salvelinus malma) in lake systems in western Alaska, the eastern and western Arctic, and south of the Alaskan Peninsula. Morphologically, each lake system contained two forms: one (Arctic char) largely confined to lake habitats and characterized by greater numbers of pyloric caeca, gill rakers, and shallower bodies, and another (Dolly Varden) predominated in adjacent stream habitats and was characterized by fewer pyloric caeca, gill rakers, and deeper bodies. MtDNA partial (550 bp) d-loop sequences of both taxa were interspersed with each other within a single ‘Bering’ clade and demographic inferences suggested historical gene flow from Dolly Varden to Arctic char had occurred. By contrast, the taxa were strongly differentiated in sympatry across nine microsatellite loci in both lakes. Our data show that the two taxa are highly genetically distinct in sympatry, supporting their status as valid biological species, despite occasional hybridization. The interaction between these species highlights the importance of the North Pacific, and Beringia in particular, as an evolutionary wellspring of biodiversity. applied directly to allopatric taxa. By contrast, putative Introduction species that come into sympatry can provide an ‘acid test’ The nature of species (their definition, origin, biogeo- of the validity of their status as distinct biological species graphy, and interrelationships) is central to evolutionary (Avise 1994). In addition, simultaneous examination biology. The biogeography of taxa has been of great of allopatric and sympatric populations of putative interest to evolutionary biologists through documenting biological species can provide critical insights into the and understanding the evolution of regional biotas and as geographic mode of speciation, i.e., whether speciation a way to resolve the distinction between, and origin of, has proceeded largely in allopatry or sympatry (e.g., species (e.g., Mayr, 1963). For instance, the biological Lynch, 1989; Bernatchez & Dodson, 1990). Such an species concept (sensu Mayr, 1963) has been criticized approach to understanding species and speciation is because the criterion of reproductive isolation cannot be manifested in emerging paradigms such as de Queiroz’s (2005) attempted reconciliation of various species con- cepts under the framework of a ‘metapopulation lineage Correspondence: E. B. Taylor, Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4 Canada. concept of species’. In de Queiroz’s model, reproductive Tel.: +1 (604) 822 9152; fax: +1 (604) 822 2416; isolation in sympatry (a so-called ‘contingent property’ of e-mail: [email protected] species) is no longer necessarily required to establish ª 2008 THE AUTHORS. J. EVOL. BIOL. 21 (2008) 1609–1625 JOURNAL COMPILATION ª 2008 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1609 1610 E. B. TAYLOR ET AL. species identity. Genetic and ecological isolation in western Pacific to the Olympic Peninsula in northwest- sympatry as measures of reproductive isolation, however, ern Washington State (USA) in the eastern Pacific are still important in establishing the evolutionary (McPhail, 1961; Behnke, 1980; Fig. 1). Brunner et al. independence among metapopulation lineages (‘species’) (2001) conducted an mtDNA-based phylogeographic and to identify different kinds of species such as ‘repro- survey of Arctic char and found five distinct mtDNA ductively isolated species’ or ‘diagnosible species’ lineages across the Holarctic. The origin of these lineages (de Queiroz, 2005). was suggested to stem from isolation within, and Fishes in the family Salmonidae constitute about 66 subsequent dispersal from, distinct Pleistocene glacial Holarctic species of salmon, trout, char, grayling, and refugia. All Dolly Varden samples, diagnosed a priori whitefish (Nelson, 2006). Salmonids have long been of using morphological and biogeographic criteria, com- interest to evolutionary biologists (e.g. Mayr, 1963, p. 39; prised the ‘Bering’ lineage found from Kamchatka north Hendry & Stearns, 2004) because they typically form to the Bering Strait and east to southeastern Alaska spatially (and sometimes temporally) discrete breeding (Brunner et al., 2001). Dolly Varden and Arctic char units that exhibit pronounced phenotypic and genetic mtDNA were paraphyletic; European, eastern North differentiation. Such differentiation occurs in a variety of American, and central Siberian Arctic char were more geographic and taxonomic contexts; from distinct taxa closely related to Dolly Varden (Beringian) mtDNA than hybridizing along a contact zone to ecotypes within a they were to the ancestral S. alpinus lineage from the taxon that are genetically distinct in sympatry (see Arctic (Canada, Greenland, and northeastern Russia) Behnke, 1972 and Taylor, 2004 for reviews). Conse- (Brunner et al., 2001; see also Oleinik et al., 2007). This quently, salmonids have provided rich material with result led Brunner et al. (2001) to conclude that the which to study the ecology, behaviour, genetics, and status of S. malma as a distinct species and one sister to biogeography of evolutionary divergence, adaptive radi- S. alpinus (cf. Phillips et al., 1995) could not be supported. ation and their relevance to speciation (e.g. Foote & In the Canadian Arctic and adjacent portions of Larkin, 1988; Jonsson & Jonsson, 2001; Redenbach & northern Alaska, Arctic char have been diagnosed as Taylor, 2002; Rogers & Bernatchez, 2006). Arguably, those lacustrine and anadromous individuals living east char (Salvelinus) have been the focus of some of the most of the Mackenzie River, as well as most of those intense and controversial studies both of the patterns (i.e. lacustrine char found west of the Mackenzie River and systematics and taxonomy) and processes in the evolu- in Alaska (Reist et al., 1996). By contrast, Dolly Varden tion of biological diversity (Behnke, 1980; Savvaitova, are usually identified as anadromous and stream-resident 1980; Coyne & Orr, 2004). Char are found in freshwater, fish west of the Mackenzie River and in Alaska (Reist estuarine, and marine environments, but breed exclu- et al., 1996). McPhail (1961) examined the morphology sively in freshwater. Across this range, there are seven of sympatric char in southwestern and central Alaska and well-accepted species (Behnke 1980). One of these found consistent differences between putative Arctic char species, the Arctic char (Salvelinus alpinus) has been and Dolly Varden, but some populations were morpho- described at many times as a ‘species complex’, i.e. a logically ambiguous. The genetic status of these sympat- collection of closely related forms each of whose status as ric populations, however, has not been examined. distinct species has at one time or another been contro- Morphological distinctions between Arctic char and Dolly versial often owing to incomplete reproductive isolation Varden are strongly tied to each putative taxon’s distinct among forms, variable levels of current and historical life-histories and habitat use (lakes vs. streams, fresh- introgression, and the presence of morphological inter- water resident vs. anadromous). It is possible, therefore, mediates (e.g. McPhail, 1961; Behnke, 1980; Savvaitova, that they represent a purely phenotypic response to 1980). Recent ecological and genetic studies have, environmental differences even within a given body of however, indicated that within the S. alpinus complex, water – a phenomenon for which char are well known the distinction between Arctic char ⁄ Dolly Varden (Savvaitova, 1980; Behnke, 1980; Nordeng, 1983; Sandl- (S. malma) and bull trout (Salvelinus confluentus) has been und et al., 1992; Sku´ lason et al., 1996). Alternatively, well established (Phillips et al., 1995; Redenbach & genetic distinction between sympatric char would pro- Taylor, 2002, 2003). By contrast, the distinction between vide the most direct test of reproductive isolation and Dolly Varden and Arctic char has remained somewhat distinct biological species status for Arctic char and Dolly more clouded, especially because multiple (up to 23 in Varden. the case of Arctic char) taxa have been described within Directly assessing the biological species status of Arctic the putative S. alpinus and S. malma lineages (Behnke, char and Dolly Varden has important implications 1980; Phillips et al., 1999; Adams & Maitland, 2007). for our
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