49 Article The charr problem revisited: exceptional phenotypic plasticity promotes ecological speciation in postglacial lakes Anders Klemetsen University of Tromsø, Breivika, N-9037 Tromsø, Norway. Email: [email protected] Received 27 October 2009; accepted 26 January 2010; published 24 May 2010 Abstract The salmonid arctic charr Salvelinus alpinus (L.) is one of the most widespread fishes in the world and is found farther north than any other freshwater or diadromous fish, but also in cool water farther south. It shows a strong phenotypic, ecological, and life history diversity throughout its circumpolar range. One particular side of this diversity is the frequent occurrence of two or more distinct charr morphs in the same lake. This polymorphism has been termed ‘the charr problem’. Similar cases are found in other postglacial fishes, but not with the extent and diversity as with the arctic charr. This review first treats the classical case, pioneered in an advanced way by Winifred Frost, of autumn and winter spawning charr in Windermere, England, and three other cases that have received much research interest in recent years: Thingvallavatn, Iceland; Loch Rannoch, Scotland; and Fjellfrøsvatn, Norway. Then a special kind of sympatry with one morph living permanently in the profundal zone, known from a few lakes in Europe, Russia and Canada and unique for arctic charr among postglacial fishes, is reviewed. Among them is a recently discovered charr at 450 m depth in Tinnsjøen, Norway, one of the few very deep lakes in the world. With examples, the concluding discussion focuses on the variation of arctic charr polymorphisms which extends from early stages of ecological segregation to cases of reproductive isolation and speciation; and on models to explain the charr problem. The exceptional diversity of arctic charr provides a unique potential for further progress in studies on ecologically driven evolution within the frames of modern theory of developmental plasticity, adaptive radiation and adaptive speciation. Keywords: Arctic charr; Salvelinus alpinus; polymorphism; behaviour; morphology; life history; profundal morphs; niche expansion; reproductive isolation; sympatric speciation; adaptive radiation; natural selection. DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 © Freshwater Biological Association 2010 50 Klemetsen, A. Introduction Oncorhynchus, the salmons and trouts of the Atlantic and Pacific regions, respectively. Salvelinus became a In 1758, Linné described the arctic charr as Salmo alpinus, taxonomic nightmare in the 20th century. A large number the trout of the mountains (Linnaeus, 1758). The scientific of species were described in Europe, Asia and America and vernacular names therefore refer charr to two different (Behnke, 1980; Savvaitova, 1980). Very many of these were landscapes, the mountains and the Arctic, and both are subsequently regarded invalid (see, for instance, Adams important for this species. The charr is adapted to cold and & Maitland (2007) for UK and Ireland). Today, five major cool water and is widely distributed in arctic and subarctic species and several species with restricted distributions regions around the world (Fig. 1), at altitude in mountains are recognised by most authors (Behnke, 1980). But on the farther south, but also in temperate lowland lakes, usually other hand and no doubt controversial, Kottelat & Freyhof living below the thermocline in the summer (Johnson, (2007) again set up a host of Salvelinus species in their new 1980). It is found farther north than any other freshwater book on European freshwater fishes. The systematics and or diadromous fish, even in lakes where the ice does not taxonomy of the genus are still problematic, but considerable break every year (Hammar, 1991; Reist et al., 1995). It is progress has been achieved by modern genetic methods. also found higher up and deeper down than any other A good example is the study by Oleinik et al. (2007) on fish in Europe, to more than 2000 m elevation (maximum the phylogeny of east Asian charr. They suggest that above 2800 m) in many lakes in the Alps and the Pyrenees north-eastern Asia was a centre of speciation in Salvelinus, (Balon & Penzak, 1980; Pechlaner, 1984; Machino, 1987, driven by periodic climate changes during the last 4 Myr. 1991), and at greater than 400 m depth in Norway (Søreide Salvelinus alpinus (L.) is particularly difficult. It et al., 2006). has a bewildering phenotypic and ecological diversity Later, Richardson (1836) established a new genus, throughout its circumpolar range, and shows extreme Salvelinus, for the charrs. The circumpolar Salvelinus life history diversity at the species, population and even became a major salmonid genus along with Salmo and individual (ontogenetic) levels. The diversity is so large that it can be asked if the arctic charr is the most variable of all vertebrates; in range, in size at maturity, in phenotype (colour, form), in behaviour, in ecology, and in life history. In this essay, I will discuss several aspects of this diversity with focus on what has long been known as ‘the charr problem’: the puzzling phenomenon that arctic charr sometimes occur as two or more distinct morphs in the same lake. Arctic charr polymorphisms were recently extensively reviewed by Jonsson & Jonsson (2001) and also treated by Klemetsen et al. (2003). Here, I will not repeat these contributions but instead, after defining the charr problem, treat more extensively the histories of one classical case, three more recent and intensively studied cases, and some intriguing cases where one morph lives permanently in deep water. Together, these cases add significantly not only to our understanding of the nature of the charr problem but also to the general discussion on Fig. 1. The Arctic charr has a wide circumpolar distribution and ecologically driven speciation. By this treatment, much of is the northernmost freshwater and diadromous fish of the world. Red colour indicates anadromy. Reprinted from Svenning & Klemetsen (2001), with permission. © Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 51 the literature that has appeared after the above reviews will problem should be restricted to the sympatric dimension, also be covered, especially in the concluding discussion. with focus on polymorphisms in postglacial time and specific lakes. Both concern the diversity of arctic charr, The problem but with different scales in time and space. The research fields around these two terms are not the same but they In his comprehensive and now classic review on the do overlap because the evolution of sympatric forms biology of arctic charr, Johnson (1980) presented the may bear upon the systematics and, ultimately, also the first historical overview of the charr problem as it then taxonomy of charr. This review is on the charr problem, but appeared in the literature. He did not use the term directly, because of the overlap with the Salvelinus complex, it will but wrote that the occurrence in the same lake of more than unavoidably also refer to literature on this phenomenon. one form has been observed throughout the geographical One of the first descriptions of different forms of range of arctic charr to an ‘extent and frequency that seems charr in the same lake is probably by Sir Daniel Fleming to be unique to this species’ (Johnson, 1980, p. 26). In who in a letter in 1665 noted that a fish known as German, the term has long been used for cases of clearly ‘case’ in Windermere, England’s largest natural lake, distinguishable, sympatric charr types in some pre-alpine is much like the charr, but spawns at a different time lakes (das ‘Saiblingsproblem’; see Dörfel, 1974). Sympatric (Frost, 1965). About a hundred years later, Pennant forms are known in other northern fishes Coregonus( , (1769, cited by Frost, 1965) remarked that the different Gasterosteus, Osmerus, Salmo), but not as widespread and seasons of spawning of charr in Windermere ‘puzzles with such a diversity as in Salvelinus. It is, perhaps, because us greatly’. So, the charr problem is an old problem. the polymorphisms are so frequent and, in some respects, spectacular and unique, that a special term is coined for Winifred E. Frost and the charr but not for other postglacial fishes. Nordeng (1983) Windermere charr referred to the char (sic) problem as the phenomenon that arctic charr frequently occur in two or three coexisting Winifred Frost (Fig. 2) was a pioneer in post-war charr forms of different sizes. I prefer the description as given research. She found that Windermere had separate (but not termed) by Johnson (1980) because other studies populations of charr that spawned at different times and have shown that there may be more than three sympatric places. She called them autumn spawners and spring morphs and because morphs may not necessarily be of spawners, after their spawning time. Her work on different sizes. Windermere (Frost, 1951, 1963, 1965) was the first clear The charr problem is sometimes confused with documentation of reproductive isolation between sympatric another term: the ‘arctic charr (or Salvelinus alpinus) charr populations. She discussed the results in relation to complex’. Behnke (1980) used it to address the speciation in her 1965 paper (even saying so in the title), taxonomic diversity of the subgenus Salvelinus, i.e. and speculated on a possible mode of sympatric speciation S. alpinus, Dolly Varden charr S. malma (Walbaum) (without using the term) in the general discussion of that and other related species. Later, he restricted the paper. This was a bold discussion at a time when Mayr’s term to all charr forms that are more closely related to allopatric speciation mode ruled in evolutionary theory. Scandinavian S. alpinus than to S. malma (Behnke, 1984). At the limnological congress in Leningrad in 1971, I For clarity, the two terms should be kept apart, as above. had the good fortune to meet Winifred Frost.