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. While I was The charr complex is about the phenotypic, systematic and waiting in the corridor outside the lecture room of one of taxonomic variation of arctic charr on, mostly, regional the many parallel sessions, she suddenly burst out of the geographic scales and time scales that may include the room and exclaimed: ‘My God, I am exhausted. You don’t whole Pleistocene (the allopatric dimension). The charr happen to have a strong drink about you, do you?’ We

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 52 Klemetsen, A.

November and in the last half of February, with no overlap. The spawning sites in the lake were also completely separate and well defined (confirmed by diving), all on hard bottom with gravel and stones. Autumn spawners consistently spawned in shallow water (1 m to 3 m depth) and spring spawners in deep water (15 m to 21 m). The tagging experiments showed that no spring spawners were recaptured on autumn spawning grounds, or vice versa (see also LeCren & Kipling, 1963). It was concluded that the charr remained separate in their spawning habits throughout their lives. The majority of spring spawners were slightly larger than autumn spawners (29 cm to 33 cm versus 28 cm to 30 cm) but the size overlap was Fig. 2. Winifred Frost (1902–1979), here in her room at Ferry high. The spawning colours were also very similar, House, FBA Windermere Laboratory, was a pioneer in charr research. Her 1965 paper will always stand as a classic study on perhaps with spring spawning males being a bit brighter. the charr problem. Photo from FBA Collection. There was a significant difference in the mean number had never met before. She was an icon in charr research; of gill rakers (15.1 versus 13.3) but the overlap was again I had given my first paper on charr the day before. I had high and individual fish could not be correctly classified. no strong drink, but took her for a cup of Russian tea, and Rearing experiments in hatchery ponds away we started talking about charr. This was so interesting from Windermere showed that progeny of both spring that I ventured to invite her for dinner that night. She and autumn spawners became sexually mature in the accepted, and we had an unforgettable evening talking autumn. The difference in spawning time was therefore about pre-war Norwegian fish biologists whom I had not maintained. It was also found that gill raker numbers never met but she knew well, and much more about charr, could be influenced by the pond environment. These especially her work in Windermere. She repeated several results did not support genetic differences between times: ‘Remember: the time and place of spawning’. autumn spawners and spring spawners. The strong Winifred Frost knew what the charr problem was about. homing to spawning sites was attributed to imprinting. In Frost (1951) gave the first description of autumn and a brief summary before the general discussion, Frost (1965) spring spawning charr in Windermere. This was followed concluded that, although some hidden genetic difference by extensive mark-recapture experiments between 1955 could not be ruled out, there was as yet no evidence that and 1960 which clearly demonstrated that mature charr imposition and imprinting were not sufficient to keep return to their specific spawning sites year after year, and the autumn and spring charr separate in Windermere. also within a year when experimentally displaced (Frost, A very interesting discussion follows this conclusion. 1963). Her main, and outstanding, publication on these fish After having referred to Regan for postglacial invasion appeared two years later (Frost, 1965). Although noting of British charr, she contrasted Svärdson’s (1951) opinion that autumn and spring spawning sites were known along that the origin of Scandinavian whitefish Coregonus( ) was the whole lake, the field material was collected in the north by multiple invasions with the interpretation by Stancovic basin: autumn spawners from two lake sites and one river (1955) that some intra-lacustrine mechanism accounted pool and spring spawners from one lake site. The sampling for the speciation of Salmo letnica (Karaman) forms in started in 1942 and continued for many years. The main Lake Ohrid, the Balkans. For Windermere, she followed result was that charr spawning was shown to take place at Stancovic and postulated that the two populations could two different times every year, peaking in the last half of have occurred by division of the original population

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 53 within the lake. She set up three possible mechanisms; 1) Partington & Mills (1988) did genetic and biometric a hypothetical physical barrier, 2) selective action dividing studies of autumn and spring spawning charr from both the breeding season and 3) delay in spawning dividing Windermere basins. They confirmed Frost’s finding that the breeding season. Under 2), selective action, some spring spawners tended to be slightly larger than autumn advantage (food supply, temperature for egg development, spawners, but with a high size overlap. Using otoliths competition for spawning ground, etc) may have favoured (Frost & Kipling, 1980, used scales), they found that spring the survival of charr which spawned early and in shallow spawners grew somewhat faster than autumn spawners water while another advantage favoured the survival of in both basins, but ages were similar. A canonical variate charr which spawned late and in deep water. Selection analysis, where gill raker numbers and caudal peduncle against those charr which spawned intermediately in time widths dominated the first two components, gave high and place could take place, so that they would virtually but not complete separation of the four spawning groups. disappear. This is nothing other than an early description A discriminant function using gill raker length and gill of disruptive selection. Under 3), delay in spawning, she raker number allowed 94 % to 96 % of the charr to be noted that late autumn spawners may have been delayed correctly sorted as autumn spawners or spring spawners. by the short days at the winter solstice and postponed the Electrophoresis confirmed the result by Child (1984) that spawning to mid-February when day-lengths are the same there were significant differences in esterase frequencies as in November. This could also imply disruptive selection. between spring and autumn spawners and differences in True, Frost writes that these possible mechanisms are malate dehydrogenase frequencies were also found. With a matter of speculation, and maintains that the factors her methods, Frost (1965) had concluded that no genetic which keep the populations apart might be accounted for differences were, as yet, found among Windermere charr, by imprinting, but she also writes that each population but she did not rule out the possibility. Partington & might continue to evolve separately from the other and Mills (1988) later concluded that there were slight genetic that it would only require a mutation in one population differences between autumn and spring spawning charr. to initiate true speciation within Windermere. Her Therefore, Frost’s speculation that sympatric splitting by discussion more than 40 years ago is impressively disruptive selection has taken place in the lake has gained clear and her contribution has long been overlooked some support in later studies. By using the discriminant in today’s debate on phenotypic plasticity (sensu West- function, Mills (1989) found that spring spawners made up Eberhardt, 1989, 2003, 2005) and sympatric speciation. only 4 % to 6 % of the charr in Windermere. Zooplankton In a later paper, Frost (1977) described the diet of was the only food found in charr caught by anglers in charr in Windermere. Feeding on charr eggs occurred the pelagic zone. There were too few spring spawners to on all spawning grounds. Outside the spawning seasons, allow direct diet comparisons but, among spawning fish, autumn and spring spawners apparently mixed in the spring spawners had higher infections of Diphyllobothrium lake. Because individual fish could not be distinguished, plerocercoids. Since these are transmitted by feeding on possible differences in diet between the populations copepods, this suggests that spring spawners tend to eat could not be studied but there were clear differences more zooplankton and, therefore, may indicate a possible between charr and the other fishes of the lake. Charr niche differentiation between the Windermere charr. almost entirely ate zooplankton, mainly cladocerans but Frost (1965) had indicated, but not tested, that autumn also chironomid and Chaoborus larvae, and emerging spawners produced larger eggs than spring spawners. chironomid pupae. The other fishes were littoral feeders. Baroudy & Elliott (1994) tested this and found that eggs and She found strong positive selection for the large cladocerans alevins from females of the same sizes were significantly Bythotrephes and Leptodora. This is an early, if not the first, smaller in spring spawners than in autumn spawners observation of selective predation in pelagic arctic charr. (mean egg sizes of 3.4 mm and 4.3 mm, respectively). The

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 54 Klemetsen, A. eggs of the spring spawners were among the smallest 1992). The benthic morphotypes have subterminal mouths recorded for arctic charr (see also Klemetsen et al., 2003). and large pectoral fins, while the pelagic morphotypes have Baroudy & Elliott also found lower survival to the juvenile terminal mouths and small pectoral fins. The differences stage of first feeding for spring spawners (3 % versus in the mouth shape between the morphotypes were found 32 %), and suggested that this may account for the small also in laboratory-raised offspring, indicating genetically proportion (Mills, 1989) of spring spawners in the lake. based differences in morphology. There appear, however, The hydroacoustic surveys by Elliott & Baroudy to be differences in the degree of morph segregation (1992), Baroudy & Elliott (1993), Elliott et al. (1996), Elliott between the pelagic and benthic morphotypes. The two & Fletcher (2001), Winfield et al. (2007a, b) and Jones et pelagic morphs, termed PL-charr (planktivorous) and PI- al. (2008) continue the work that Winifred Frost started charr (piscivorous) probably belong to a single population and are important because the well-studied and unique and differ mainly by asymptotic size (PI-charr being the Windermere charr is threatened by eutrophication largest), probably influenced by the size differences of and competition from a diverse and changing their prey (Snorrason et al., 1989, 1994). The two benthic fish community (Elliott et al., 1996; Pickering, morphs are phenotypically more different, with differences 2001; Winfield et al., 2007b; Jones et al., 2008). both in measurable characters, gill raker numbers and colouration in addition to size (Sandlund et al., 1992). Three European hotspots The large-benthic (LB)-charr spawns in July–August in cool underwater springs mostly in the northern part of Among the many cases of sympatric charr morphs that are the lake (Skulason et al., 1989) while the pelagic morphs known (Johnson, 1980; Jonsson & Jonsson, 2001; Klemetsen spawn later (peaking in October) in the littoral around the et al., 2003), the results from Thingvallavatn (Iceland), Loch lake. The spawning time of the small-benthic (SB)-charr is Rannoch (Scotland) and Fjellfrøsvatn (Norway) have protracted and overlaps in time and place with all the other contributed significantly not only to the understanding of morphs (Skulason et al., 1989, 1999). Even with overlap the charr problem, but also to contemporary research on in the time of spawning, segregation may be maintained ecological speciation in general. These low-production by aggressive behaviour of LB spawners against possible lakes of similar postglacial ages (at least 10 000 years) have SB intruders (Sandlund et al., 1992), although limited all been studied intensively in recent years. sneak matings may occur (Sigurjonsdottir & Gunnarson, 1989). Reproductive isolation is, therefore, largely but Thingvallavatn, Iceland not completely maintained between morphs by the time and place of spawning and behaviour, but coefficients of The occurrence of different charr morphs in Thingvallavatn genetic similarity indicate some gene flow between the was first reported more than a hundred years ago morphs, especially because the long spawning period may (Sæmundson, 1904) and their ecology and evolution have allow a few SB-charr males to mate with females of the been studied intensively since the 1980s. Sandlund et al. larger morphs (Volpe & Ferguson, 1996). (1992) presented the knowledge acquired during the first Thingvallavatn is situated in a neovolcanic area that has decade, and a series of important papers have since then given the lake a highly diverse littoral habitat of spatially been published (see Skulason et al., 1999; Snorrason & complex lava substratum with innumerable crevices and Skulason, 2004; and references therein). The lake is unique interstitial spaces (cf. Jonasson et al., 1998). This habitat in having two superior morphotypes (pelagic and benthic), supports a benthic community with high diversities each with two morphs, giving a total four sympatric and densities of macroinvertebrates, where Lymnaea morphs (for Thingvallavatn, the hierarchical distinction gastropods are important as fish prey because of their large between morphotype and morph follows Sandlund et al., size (Malmquist et al., 2000). The SB-charr shows a unique

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 55 adaptation to this unusual habitat. Its small size allows conservative and possibly limited by the available data. penetration into the three-dimensional spaces of the lava Although the genetic analyses are somewhat conflicting, to feed on the food resources that are found there. The LB- all show that the Thingvallavatn charr morphs are closely charr is too large to have access to this food supply. Both related and have a monophyletic origin (Wilson et al., 2004). morphs feed on Lymnaea (Malmquist et al., 1992), but the Several phenotypic differences between the LB-charr only from the surface of the substratum. LB-charr Thingvallavatn morphs are probably partly genetically also moves deeper down along the bottom while the SB- based. In an experiment with wild-caught fish, Malmquist charr is concentrated in the surf zone of the littoral where the (1992) found clear differences in feeding behaviour between interstitial lava spaces are best developed. Therefore, these SL-charr and SB-charr that could indicate genetically based two charr morphs which utilise similar prey are ecologically differences. Skulason et al. (1993) also found consistent segregated by differential use of a spatially complex space differences in the feeding behaviour between progeny (Snorrason et al., 1989, 1994). Small benthic charr similar to of the charr morphs, and concluded that the differences the SB-morph of Thingvallavatn are found in several other must be genetically based since all experimental fish were habitats with three-dimensional lava substratum in Iceland offspring raised in a common environment. Apart from (Sigurdsteindottir & Kristjansson, 2005). One of these, a a somewhat unexpected reluctance of young PL-charr pool in a tributary to the outflow river from Thingvallavatn to feed on plankton, the progeny showed behaviours that has been isolated from the lake for 9600 years, had that correlated with their niche segregation in the small benthivorous charr that were very similar to the wild. This study is important because it was the first to SB-charr. There are, however, differences in the structure demonstrate that phenotypic differences in behaviour of the head, indicating that further selection powered by among closely related polymorphic fishes can have a subtle local differences, not yet disclosed, can operate genetic basis. This immediately indicated that selection in these lava habitats (Sigurdsteindottir & Kristjansson, on behaviour had taken place in an early phase of the 2005). This study shows that Iceland’s special geology process of ecological speciation. Furthermore, and also promotes parallel adaptation to a resource niche that is in carefully planned experiments with laboratory-raised not developed like this anywhere else, but also that spatial offspring in common environments, it was shown that isolation can give further local adaptation in these habitats. life history traits, body size and skeletal development Early genetic analyses by allozymes (Magnusson & had genetic components that differed between Ferguson, 1987) and mtDNA (Danzmann et al., 1991) failed morphs (Skulason et al., 1996; Eiriksson et al., 1999). to demonstrate significant genetic differentiation between Several general papers have drawn heavily on the the Thingvallavatn morphs, but the data suggested that results from Thingvallavatn. Skulason & Smith (1995) SB-charr were slightly more divergent (Danzmann et al., and Smith & Skulason (1996) discussed the importance 1991). Later genetic examination (mtDNA, minisatellites) of resource polymorphisms in vertebrate evolution found some differences between, but not within, the and Skulason et al. (1999) and Snorrason & Skulason morphotypes (Volpe & Ferguson, 1996). SB-charr were (2004) focused on sympatric evolution of northern different from PL-charr but not from PI-charr, while postglacial fishes, with emphasis on arctic charr, LB-charr were different from both pelagic morphs. The particularly from Thingvallavatn. Inspired by the differences were small, and Volpe & Ferguson suggested unique four-morph situation in Iceland’s largest lake, that the morphs had segregated sympatrically in the lake, these contributions put the charr problem on the agenda not by repeated postglacial invasion. By genotyping at six of ecologically driven speciation in a significant way. microsatellite loci, Wilson et al. (2004) did not find direct support for sympatric populations in Thingvallavatn, but added that their estimation of putative populations was

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 56 Klemetsen, A.

Loch Rannoch, Scotland showed deterministic growth, while piscivorous charr, that feed on a wide size range of prey, did not. Relatively little was known about arctic charr in Scotland Two important papers based on experiments a few decades ago (Maitland et al., 2007) but a number of with laboratory reared offspring from the benthic and new studies have substantially increased our knowledge of pelagic morphs were published in 2002. First, Adams & Scottish charr. Charr have been verified in about 150 lochs Huntingford (2002a) demonstrated that offspring of the in recent years but the number is likely to be significantly two morphs had differences in head morphology that higher (Maitland et al., 2007). Since the demonstration matched the differences previously found in wild fish, of sympatric morphs in Loch Rannoch by Gardner and that the differences increased allometrically with size. et al. (1988) and Walker et al. (1988), research on this These findings showed that the phenotypical differences polymorphism has contributed much to modern studies between the morphs were partly inherited. Then Adams on the charr problem. Gardner and Walker and their & Huntingford (2002b) found that the benthic morph was colleagues found that the lake had two morphs of charr, able to handle larger food particles in relation to gape size one a claret coloured pelagic morph and the other a pale, than was the pelagic morph. When offered live benthos cryptically coloured benthic morph. Their sizes overlapped (Tubifex worms) and plankton (Artemia phyllopods), extensively, but there were clear differences in colour offspring of the benthic morph were more likely to take and morphology. The pelagic morph was planktivorous benthos, while offspring of the pelagic morph were more and the benthic morph was benthivorous. Their times likely to take plankton. These results indicated selection of spawning overlapped, but separate spawning places for genetic differences in morphology and behaviour were indicated, with the benthic form spawning in the between the Rannoch morphs. Adams & Huntingford estuary of the inlet stream, the River Gaur, and the other (2002b) proposed that heterochronic growth (changes in form along the shores of the loch. Hartley et al. (1992) developmental timing: see Gould, 1977) is the mechanism found genetic differences using allozymes and mtDNA resulting in the divergence of the trophic anatomy. that supported the proposal by Walker et al. (1988) that the In a later experiment Adams & Huntingford (2004) benthic and pelagic morphs were reproductively isolated. tested the relative effects of morph (benthic and pelagic) and Later, Adams et al. (1998) extended the ecological and rearing environment (laboratory and wild) on phenotypic morphological analyses and found that there were three variance. They found a strong underlying genetic (morph) sympatric morphs in Loch Rannoch. The study confirmed effect in the laboratory treatment, but the overall effect the presence of a planktivorous, brightly coloured pelagic of environment was considerably larger. Thus, rearing morph that spawned in the littoral, particularly at Dall Bay. environment explained more variation than did morph in In addition, they found that the cryptically coloured charr six out of nine head anatomy variables. Jaw length, which consisted of two morphs, clearly separated by diet and is functionally important for foraging, showed the greatest head measurements: one less robust morph was a benthos- phenotypic variability. They concluded that a phenotypic feeder and spawned in the Gaur inlet while the more plasticity model (West-Eberhard, 1989; Skulason et al., robust morph was piscivorous and spawned at the Dall 1999) explained the benthic–pelagic polymorphism in Loch Bay site. Adams et al. (1998) concluded that the distinct Rannoch well, and that evolution of this polymorphism has phenotypic differences between the morphs, particularly diverged to a point where the gene-pool is now segregated. in the head-shape, were so great that ontogenetic transfer The remarkable results from Loch Rannoch between them was unlikely. In a later paper, Fraser et al. inspired a series of other studies on charr across (2007) applied arguments from optimal foraging theory Scotland, and polymorphisms were disclosed in to predict body size constraints in the three morphs. The several new lochs and catchments (see Adams et al., benthic and pelagic charr, both feeding on small prey, 2006, 2007, 2008; and references therein). Together,

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 57 these studies have placed the charr polymorphisms spawning colour of the profundal charr is also a genetic and phenotypic plasticity in Scottish lochs, along with trait, probably selected for in the profundal environment. similar research in Iceland, in the forefront of present Genetically based differences were also found in day research on ecologically driven incipient speciation. behaviour. The morphs have distinct diet niches in the lake. The littoral morph feeds on pleuston, plankton Fjellfrøsvatn, Norway and littoral benthos while the profundal morph feeds on profundal benthos (Klemetsen et al., 1997; Knudsen et Modern Norwegian research on the charr problem started al., 2006). Under identical conditions, naïve offspring (no with studies in an open (anadromous) system in northern Norway (Nordeng, 1983), a west coast lake (Hindar & Jonsson, 1982; Jonsson & Hindar, 1982) and in high altitude lakes in northern Norway (Klemetsen & Grotnes, 1975; 1980), and continued with studies on several systems around the country (Jonsson & Jonsson, 2001; Klemetsen et al., 2003). In 1992, an unusual charr morph was discovered in Fjellfrøsvatn, northern Norway. The dominant morph in the lake is of a common charr phenotype that spawns in shallow water in October. In contrast, the new form is very small (up to 14 cm) and cryptic (Fig. 3, upper panel) and spawns in deep water in February–March, under thick snow and ice (Klemetsen et al., 1997; Knudsen et al., 1997). The clear differences in time and place of spawning immediately suggested reproductive isolation. The morphs were termed littoral and profundal charr after their spawning places. An experimental study revealed significant differences between the morphs in tail, fin, head and mouthpart measurements, both for wild fish and for offspring reared in the laboratory (Klemetsen et al., 2002a). Offspring of the profundal morph had a specific growth rate that was more than twice that of the littoral morph. This was unexpected because of the very slow growth of their wild parents but the result was that the laboratory offspring grew to sizes very Fig 3. The subarctic lake Fjellfrøsvatn, Norway, has two much larger than their wild parents (Fig. 3, lower panel). reproductively isolated arctic charr morphs, termed littoral charr The study concluded that the differences between the and profundal charr after their spawning places. Littoral charr spawn in shallow water in the autumn while profundal charr Fjellfrøsvatn morphs in morphometry and growth capacity spawn in deep water five months later, under thick ice and snow. had a genetic basis. For the profundal charr, the better Genetic differences are found by microsatellite analysis, and also growth capacity may be an adaptation to restricted food in morphology and behaviour. Upper panel: females and males of both morphs in spawning colours. Lower panel: mother and resources. At maturity, offspring of the profundal morph son; demonstrating the surprisingly high capacity for growth had pale spawning colours like the wild parents (Fig. 3) that profundal charr showed when given enough food in the laboratory. The son had pale spawning colours like the mother. while offspring of the littoral morph became very brightly The high capacity for growth and the pale spawning dress are coloured on the same food. This indicates that the cryptic probably genetic traits selected for in the profundal environment. Photos by Rune Knudsen.

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 58 Klemetsen, A. experience with live prey, only feed pellets) of the littoral driven incipient ecological speciation in Fjellfrøsvatn, with morph were more active, more aggressive and more expansion to new resources (niche invasion, sensu Schluter, pelagic than naïve offspring of the profundal morph 2000), and not by subdivision of an ancestral broad niche. while naïve offspring of the profundal morph were more By including winter sampling under the ice, Amundsen effective in eating live chironomid larvae (Klemetsen et al., et al. (2008) completed the understanding of the seasonal 2002a). In another experiment, the behaviour associated and ontogenetic patterns of resource utilisation by the with typical prey of the littoral morph was tested, again two morphs. This study confirmed that profundal charr comparing naïve offspring of the morphs under identical remain in the profundal zone at all seasons and for their conditions (Klemetsen et al., 2006). As predicted, offspring entire lives. In contrast, littoral charr live in shallow water, of the littoral morph were more effective in approaching close to the ice, during the winter but perform a brief dive and taking live pleuston (Gerris pond skaters), plankton to deep water at, or immediately following, the ice-break. (Daphnia) and littoral benthos Gammarus ( amphipods). Then most of the population moves back to shallow water It was concluded that divergent adaptations in within a few weeks. Some young charr remain in deep feeding behaviour had developed by natural selection. water during the ice-free season but all have moved up Genetic differences between the morphs were to the littoral when the ice again forms on the lake. Apart confirmed by microsatellite DNA analysis by Westgaard from a slight overlap due to eating the benthic cladoceran et al. (2004) and Wilson et al. (2004). The results were Eurycercus in the summer, the diets of the similarly sized strengthened by the fact that the two studies analysed profundal charr and young littoral charr are different different microsatellite loci and, together with the when co-occurring in deep water. Deep water sampling differences in morphometry and behaviour, strongly revealed an interesting difference between the morphs. confirmed the hypothesis of reproductive isolation. When hauled to the surface, profundal charr had highly Wilson et al. (2004) also indicated that the Fjellfrøsvatn inflated swim bladders and seemed unable to release the morphs may not have a monophyletic origin. gas even when given an opportunity to decompress at 5 The littoral morph has ontogenetic and seasonal m depth. Young littoral charr never had such problems. habitat shifts, and some young fish occur in deep water Apparently, profundal charr are unable to regulate along with the profundal morph during the ice-free season the volume of their swim bladders by letting out gas (Knudsen et al., 2006). More than 10 years of observations through the pneumatic duct. Amundsen et al. (2008) have, however, shown their diets to be consistently pointed out that if this is an adapted trait in profundal different. Profundal charr feed on soft bottom resources charr, it would have a significant role in their evolution, (chironomids, Pisidium bivalves, benthic copepods, because, if a fish moves to shallow water, buoyancy Eurycercus cladocerans) while young littoral charr mainly would make swimming back to deep water impossible. take zooplankton in deep water. In four other lakes with The pronounced dimorphism between the littoral and monomorphic charr populations (no profundal charr profundal morphs of Fjellfrøsvatn differs from the usual morph), young charr perform similar habitat shifts and pattern of littoral benthic–pelagic resource segregation. feed on plankton in deep water. The profundal morph The littoral morph does, however, exploit both the pelagic in Fjellfrøsvatn therefore utilises a food resource that and the littoral-benthic food resources. In the lake Store neither the littoral morph nor comparable monomorphic Rennen, central Norway, Bjøru & Sandlund (1995) had populations exploit. These long-term studies by a group found that charr caught in the pelagic zone and the littoral from the University of Tromsø have shown that the clear zone in late summer had different diets and also differences polymorphic structure and foraging specialisisms of charr in head and fin morphology. Using an individual fish in the lake are stable over time. Knudsen et al. (2006) approach, Knudsen et al. (2007) analysed trophic niche suggested that intraspecific resource competition has (habitat and diet) and trophic morphology (body form

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 59 and head structure) in Fjellfrøsvatn. The same analyses Comparison were conducted on charr from Lille Rostavatn, another lake in the Målselv river system. The lakes are of similar No charr polymorphisms have been studied as intensely size and morphometry but their fish communities differ, as Thingvallavatn, Loch Rannoch and Fjellfrøsvatn, and all with only charr and brown trout in Fjellfrøsvatn and six three cases combine ecological, morphological, behavioural, fish species in Lille Rostavatn. It was found that individual genetic and experimental approaches like no other studies. Fjellfrøsvatn charr specialised in benthivore or planktivore The results have demonstrated interesting similarities niches that correlated with their morphological differences but also differences. Thingvallavatn is no doubt the best while the charr in Lille Rostavatn were restricted to studied and best known of all charr polymorphisms. It is planktivory and showed no morphological differentiation. also the only case with four sympatric morphs. The main Therefore, incipient steps towards evolution of a classic split is along the benthic–pelagic axis, and then each main pelagic–benthic divergence were found in the autumn morphotype is split into two morphs. From an ecological spawning population of Fjellfrøsvatn, but not in the speciation view, it is exceedingly interesting that the niche other lake. It appears that strong competition from other pushing of the small benthic charr into the food and habitat fishes, particularly burbot Lota lota (L.), excludes charr resource of the lava surf zone has also developed elsewhere from the benthic food resources of Lille Rostavatn. This in Iceland. Reproductive isolation appears to be nearly but is in accordance with the later finding by Claessen et al. not fully complete among the Thingvallavatn morphs and (2008), based on the material of Alekseyev et al. (1998, 2002) the genetic analyses conclude that they are closely related from Transbaikalian lakes, that there is a negative relation and have a monophyletic postglacial origin. There are between the number of other fish species and the number important genetically based differences in morphology of charr morphotypes. In a new study from Fjellfrøsvatn, and behaviour, but also high levels of phenotypic plasticity Knudsen et al. (2010) related recent (diet and habitat) and and different degrees of divergence among the morphs. long-term niche use (accumulation of food transmitted The situation in Loch Rannoch is similar to Thingvallavatn, parasites that tracks prey selection backwards) to the with the main divergence being along the pelagic–benthic functional morphology of individual fish. High inter- axis, but different in having three morphs that, moreover, individual consistency of narrow niches (planktivorous have a high size overlap. The clearest, and best studied, or benthivorous) was evident throughout the ontogeny segregation is between the planktivorous and benthivorous of the charr, indicating a low degree of switching both morphs but the piscivorous morph also has significant in habitat utilisation and feeding strategy of individual morphological differences. Reproductive isolation fish. Differences in their trophic morphology (body form, seems to be well developed, with distinct differences in head robustness) correlated with their diet niches. Thus, the times and places of spawning, and the benthic and in Fjellfrøsvatn, there is a possible adaptive radiation into pelagic morphs are genetically distinct, possibly even a three-morph situation: one old and well-segregated with a diphyletic origin. The clearer genetic differences profundal morph and, among the littoral autumn indicate that incipient ecological speciation between the spawners, two incipient forms (benthivore and planktivore planktivorous and benthivorous morphs has come further ecotypes). In a tagging experiment, Figenschou et al. than in Thingvallavatn. In Fjellfrøsvatn, the differences (2004) found high spawning site fidelity in male littoral between littoral benthos feeders and plankton feeders in the charr in the lake. It remains to be tested if this fidelity is autumn spawning population, although significant when coupled to the incipient ecotypes in the littoral morph. examined at the level of the individual fish, seem to be in an incipient phase with high phenotypic plasticity intact. In contrast, the profundal morph is markedly segregated, with complete reproductive isolation in time and place,

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 60 Klemetsen, A. expansion into a separate resource niche, clear genetically and 60 m to 80 m (Constance) depths. Small, soft-bottom based differences in behaviour and morphology, and prey (turbellarian cocoons, chironomids, crustaceans, distinct genetic differences that may not be of monophyletic Pisidium bivalves) were the food resource in both lakes. origin. The profundal Fjellfrøsvatn morph seems to have The spawning times of these profundal charr were not advanced far towards speciation while the littoral-pelagic well known, but probably extended to between July and divergence is still in a very early phase. February (or even all seasons) in both lakes (Freyhof & Kottelat, 2005). The pneumatic ducts were probably Profundis vivens dysfunctional because the swim bladders expanded when the fish were taken to the surface. The co-occurring morph Permanent life in deep water is unusual among in Lake Constance was more brightly coloured, did not polymorphic postglacial fishes, but a few cases are found live as deep as the profundal morph and grew to larger in charr. Some of these have been known for a long time sizes (up to 40 cm versus less than 28 cm; Dörfel, 1974). but several interesting cases were recently discovered. There were distinct morphological differences in gill raker Profundal charr morphs are interesting not only because numbers and head morphology. Their times and places they deviate from the littoral benthic–pelagic norm but also of spawning were different. The co-occurring morph because their divergence seems to have developed further in Lake Neuchatel, also now extinct (Freyhof & Kottelat, and become more stable. 2005), appeared to have been a large piscivorous charr. Deep, central European pre-alpine lakes provide the The lake is now stocked with charr from Lake Geneva. classic cases. The first descriptions go back to the start of Attersee originally had three charr morphs, but the 20th century. Freyhof & Kottelat (2005) list several lakes only profundal charr were found when Brenner (1980) with deep-living charr (Tiefseesaibling) in the Danube sampled by net between 40 m and 130 m depths. Like and the Rhine basins but remark that many of them are other profundal charr morphs in pre-alpine lakes, this is a not well studied and may be cases of slow-growing fish small-sized (up to 25 cm, with the bulk of the catch 13 cm (Schwarzreuter) that belong to the other charr population to 20 cm) and pale-coloured fish. The main spawning of the lakes. Clear polymorphisms with one profundal sites were between 40 m and 60 m depths and the main morph were found only in the lakes Neuchatel (Quartier, spawning period was July to November, but sexually 1951), Attersee (Brenner, 1980) and Constance (Konstanz, mature specimens were present at all seasons. Mature Bodensee) (Dörfel, 1974). Also, Ammersee has a real deep gametes were found in all months of the year, and fish water charr, but this lake has no charr polymorphism. eggs were found in the stomachs throughout the year. The Freyhof & Kottelat (2005) described it as a new species, and summer diet was zooplankton and the autumn and spring also recognise the Neuchatel and Constance profundal diet was chironomids, oligochaete cocoons and amphipods. forms as separate species (see also Kottelat & Freyhof, In Norway, the first charr polymorphism with one 2007). The profundal forms in Neuchatel and Constance morph living permanently in deep water was described are now extinct due to eutrophication. Behnke (1980) said by Hesthagen et al. (1995) in Sirdalsvatn, a deep (165 that it would be tragic if the unique deep charr of Lake m) fjord-lake in the south-western part of the country. Constance died out; by sad irony, this was probably already Mature profundal charr in the lake are pale-coloured, the case when that was written (Freyhof & Kottelat, 2005). have parr marks and are less than 25 cm long. The other The profundal charr of Neuchatel and Constance morph is colourful and grows larger. There are significant appear to have been quite similar in phenotype and ecology differences in gill raker counts between them, and Hindar (Quartier, 1951; Dörfel, 1974). Both were profundal, cryptic et al. (1986) found that they were genetically distinct by and small fishes (usually less than 20 cm), living permanently allozyme analysis. Profundal charr were caught from in deep water and spawning at 100 m to 150 m (Neuchatel) 16 m to 82 m depths, with the majority deeper than

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 61

32 m; while the other morph occurred from shallow water. Isotope analyses (O’Connell et al., 2005; Power et water down to 32 m. Their spawning depths were well al., 2005) showed significant signature differences between segregated (below 55 m and above 32 m, respectively). the two morphs. This showed that their foraging niches Ripe profundal charr were caught throughout the year, were persistent over time, confirming the ecological but the majority spawned from July to September. This segregation of the profundal Gander Lake charr morphs. was the first observation of a summer-spawning charr in Until recently, Sirdalsvatn and Fjellfrøsvatn were the Scandinavia. The littoral morph spawned in November. only known charr polymorphisms in Norway where There appears to be an almost complete segregation in one morph is a permanent deep water form. Then, in time and place of spawning between these sympatric charr 2004, a remarkable new case was found, more or less by morphs. It is remarkable that the profundal morphs of coincidence (Søreide et al., 2006). In 1944, a railway ferry Sirdalsvatn and Fjellfrøsvatn (see above) spawn at opposite that carried a load of heavy water destined for trials with seasons, one in the summer and the other in the winter. atomic reactors in Germany was sunk by sabotage in The large (113 km2) and very deep (288 m) Gander Tinnsjøen, county Telemark. Tinnsjøen is 460 m deep Lake in Newfoundland was found to hold two discrete and the ferry was discovered, located at about 400 m morphs of arctic charr (O’Connell & Dempson, 2002). in 1993. With cameras on a remotely operated vessel They differed in colour (pale and dark), meristic characters (ROV), Søreide et al. filmed the wreck in 2004. To their (fin ray, gill raker and vertebra counts) and size. The size astonishment, the cameras picked up several small white distribution of dark charr was 11 cm to 49 cm, while the fishes on and around the wreck. More than 30 fishes few pale charr were all small (9 cm to 19 cm). Pale charr were observed at 400 m to 450 m depths. They were were caught along the bottom from 20 m to 100 m depths, always on the bottom, sometimes half submerged in the while dark charr were taken from shallow water and soft sediments Fig.( 4). When disturbed by the ROV, they down to 100 m, with a tendency to move to cool water swam for a short distance, leaving a track in the sediment. below the thermocline in the summer. A few dark charr, Their sizes were estimated to be 5 cm to 15 cm. Additional but no pale charr, were also caught in the pelagic zone. The field work was organised in 2005, and this time the ROV diet of dark charr was dominated by benthic invertebrates (mainly littoral insects and gastropods) and fish (mainly sticklebacks). Plankton was not important. Unidentified insect remains (but, somewhat puzzling, also Coleoptera in one fish), were found in the stomachs of two pale charr. O’Connell & Dempson (2002) tentatively concluded that Gander Lake has two ecologically discrete charr forms, with the pale charr being confined to deep water. Later studies confirmed the ecological distinction between these sympatric morphs, with the pale charr as a true profundal morph, living exclusively in deep water and largely deeper than 50 m and all the way to 280 m, where five specimens were caught (O’Connell et al., 2005). One dark charr was also taken at this depth. These catches were Fig. 4. An unknown charr, possibly a new profundal morph, was recently discovered at 400–450 m depths in Tinnsjøen, county the deepest ever recorded for arctic charr at the time. The Telemark, Norway. Tinnsjøen is one of very few lakes worldwide new and extensive material confirmed the differences in that are deeper than 400 m. This photograph was taken by a Remotely Operated Vessel ROV in 2004. The fishes were small, diet. Pale charr had a dominance of chironomid larvae in almost colourless and somewhat burrowed in the sediments. their stomachs, particularly in fishes caught in very deep Two live specimens were brought to the surface by another ROV search in 2005. Photo by Fredrik Søreide.

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 62 Klemetsen, A. was fitted with a pump specially constructed for catching Newfoundland, both sympatric and allopatric hypotheses fish. Two fishes, 3.5 cm and 7 cm long, were caught. Both are possible for Gander Lake (Gomez-Uchida et al., 2008). were alive and did not have swim bladder problems when In Transbaikalia, Russia, Alekseyev & Pichugin (1998) brought to the surface, and one lived for a month after described a very distinct profundal morph living in the catch. They had little pigment, faint parr marks, very sympatry with two other morphs, one piscivorous and slim bodies, and large heads with small eyes and tubes one planktivorous, from Lake Davatchan. The profundal protruding from the nostrils. The eyes appeared to be morph was small (up to 20 cm) and of a uniform silvery partly degenerated because a proper eyeball was lacking. colour, without parr marks and light spots. Meristic Phenotypic and preliminary genetic analysis confirmed (gill raker, scale, pyloric caeca and vertebrae counts) and that these fish were charr. Two other sympatric charr morphological (head and body measurements) traits were morphs are previously known from Tinnsjøen (Hindar significantly different from the sympatric morphs. All et al., 1986). Søreide et al. (2006) tentatively suggested profundal charr were caught in deep water, mostly in 35 m that the extreme profundal charr evolved postglacially to 45 m depths. A footnote added when the paper was in in the lake, and may possibly be different from the two press states that spawning (indicated by running females) other morphs. Further studies are needed to test this. took place in deep water in late June. Transbaikalia is At the fifth charr symposium in Reykjavik, Iceland interesting because it is the southernmost arctic charr in 2005 (Noakes, 2008), Brian Dempson presented a region in Siberia. Based on a study of 21 lakes, Alekseyev video recording that showed the movements of small et al. (2002) considered this region to be important for charr in deep water in Gander Lake. The fish left tracks research on charr evolution because of an unusually high behind them as they moved in the soft sediments, and meristic variation in charr and a level of polymorphic they prodded their head and mouth into the sediment, divergence that differs much among lakes. The material possibly in search of burrowing prey. Their colour and of Alekseyev and co-workers was utilised by Claessen et size indicated that these were pale charr, the Gander al. (2008) for an empirical test of a model for evolution of profundal morph. The behaviour was strikingly similar to polymorphism and speciation in sexual populations. For what Søreide et al. (2006) saw in their video recording of a given number of co-existing fish species, they found that the peculiar deep water charr in Tinnsjøen. At about the the level of charr polymorphism increased with a crude same time, therefore, modern technology demonstrated estimate of lake volume. Alekseyev et al. (2002) found the similar behaviour of two recently discovered profundal Lake Davatchan profundal charr to be the most divergent charr morphs from two distant but very deep lakes. of the Transbaikalian morphs. A co-occurring morph was Microsatellite DNA analysis showed clear reproductive almost exclusively planktivorous. The profundal charr isolation between the pale and dark morphs of Gander took much plankton, but also benthos, in the summer Lake (Gomez-Uchida et al., 2008). Compared to other and switched to a benthos diet in the autumn. Emerging microsatellite analyses of arctic charr (Gislason et al., 1999; insects and surface food were not exploited. Alekseyev Westgaard et al., 2004; Wilson et al., 2004), the genetic et al. (2002) concluded that an independent parallel divergence was moderate to strong, and they found that sympatric origin was most likely for the Transbaikalian mutation was equal to or more important than drift in charr and that reproductive isolation has evolved in creating this polymorphism. Based on expected mutation several cases, including the Davatchan profundal charr. rates and generation times, they also found that part of The research on this very distinct deep water charr adds the differentiation could precede the last glaciation. If so, importantly to our restricted knowledge on life in the deep. this might imply a possible unique colonisation of Gander Despite the great geographic distances between Lake, but until a better search is done in other deep lakes in them, these profundal morphs are strikingly similar. All are small-sized and pale, even when sexually mature,

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 63 and they resemble each other in body form and head but has since been difficult to apply to non-anadromous morphology. Their habitat is invariably at the bottom polymorphisms. Nordeng’s contribution now stands on soft sediments, their resource niches are similar as a significant classic study on charr diversity because (soft bottom benthos, rarely deep plankton), and all are of its thorough field approach combined with extensive reproductively isolated by time and place of spawning hatchery experiments, but it only partly solved the problem. from their co-occurring morphs. Across the Holarctic, Essential theoretical steps forward came with the profundal charr appear to be more distinct and more contributions of Adams (1999) and Skulason et al. uniform than parallel trophic morphs in the more (1999) because they first pointed out that there is large common littoral benthic–pelagic charr polymorphisms. variation among cases in the phenotypic expressions of charr polymorphisms and, second, suggested models Concluding discussion to explain this variation. Taking inspiration from the long-term studies by John Thorpe and colleagues (see Our understanding of the charr problem has come a Thorpe, 1986, 1994, and references therein) on different life long way since sympatric charr forms were first noted history outcomes for young Atlantic salmon Salmo salar in Windermere more than 300 years ago. The modern L., Adams (1999) suggested that there are two different approach to the problem started with Winifred Frost’s mechanisms behind charr polymorphisms: ontogenetic studies in the 1940s, also in Windermere. The Windermere and genetic transformations. In the ontogenetic model, charr are unusual in showing minor morphological and both horizontal (within lifetime) and vertical (over ecological differences despite their different times and generation) transformations of sympatric morphs occur places of spawning (Mills, 1989). The many new cases of (Fig. 5). This means that individual fish can change documented charr polymorphisms confirm the unique from one morph expression and life history strategy to position of Windermere. Few lakes have sympatric another and that within morph matings can give rise to charr with such clear-cut reproductive isolation and few, all morphs, as shown in rearing experiments by Nordeng if any, lakes have sympatric charr that are so similar in (1983). This does not preclude all genetic influence, but size, phenotype and diet. Most other lakes have benthic– means that there are no hard deterministic effects such pelagic trophic polymorphisms while Windermere has that one morph always gives rise to offspring of the same two planktivores. Altogether, 16 fish species have been morph. In contrast, in the genetic model, no horizontal recorded in the lake (Pickering, 2001), resulting in a dense or vertical transformations take place (Fig. 5), as shown and diverse littoral fish assemblage that probably does not by the results from Thingvallavatn and Loch Rannoch. allow a benthivorous charr type to evolve. Another rare Anadromous systems (e.g. Kristoffersen et al., case of two planktivorous charr morphs was described by 1994; Strand & Heggberget, 1994; Radtke et al., 1996; Samusenok et al. (2006) in a nameless Transbaikalian lake Rikardsen & Elliott, 2000) but also migratory freshwater situated at 1766 m a.s.l. The high elevation (possibly the systems (Näslund, 1990), where there are size-frequency highest natural charr lake in the world) probably causes a polymorphisms, probably develop by ontogenetic, paucity of food other than plankton, to which both morphs environmentally-induced mechanisms, and often have adapted. differences in food and growth. Piscivorous morphs are Important progress has been achieved since Frost’s found in Thingvallavatn, Loch Rannoch and several other pioneering work. A remarkable contribution came polymorphic examples. In lakes where charr are the only from Salangen, subarctic Norway, when Nordeng fish, the piscivores are cannibalistic (e.g. Skreslet, 1973; Reist (1983) offered a ‘solution’ (his apostrophes) to the charr et al., 1995; Svenning & Borgstrøm, 1995; Hammar, 2000; problem. His model explained the complicated mixture Finstad et al., 2001; Power et al., 2008). Many piscivores and of anadromous and resident forms in Salangen quite well, cannibals probably develop ontogenetically, as shown in

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 64 Klemetsen, A.

Fig. 5. This model cleared up much of the early confusion about the mechanisms behind the charr problem because it distinguished between ontogenetic (upper panel) and genetic (lower panel) morph transformations. Most anadromous and piscivorous charr morphs probably are cases of ontogenetic transformations while advanced littoral-benthic, pelagic and profundal-benthic morphs are cases of genetic transformations. Redrawn and reprinted, with permission, from Adams (1999). Artwork by Frøydis Strand. long-term whole lake manipulations of population density genetically based traits that distinguish them from their in Little Nayuk Lake, arctic Canada (Johnson, 1983) and sympatric morphs, and hatchery (Amundsen et al., 1999) Takvatn, northern Norway (Klemetsen et al., 2002b; Persson and field (Svenning & Borgstrøm, 2005) experiments have et al., 2007). By using stable isotope analysis, McCarthy et demonstrated that there may be strong genetic influence on al. (2004) convincingly demonstrated that one morph in cannibalistic behaviour. In polymorphic cases, attainment Loch Ericht switched from benthos to fish feeding at a size of large size through ontogeny does not necessarily involve threshold of 17 cm. Likewise, Byström (2006) in an elegant, piscivory. The lake Øyangen at Bear Island in the Barents detailed study in Ruozujaure, northern Sweden, showed Sea is dominated by charr that grow to large sizes (several that giant charr cannibals developed by recruitment pulses kg) on a diet of the benthic crustacean Lepidurus arcticus in the population. On the other hand, the piscivorous Pallas while most charr (apart from a few large cannibals) charr morphs in Thingvallavatn and Rannoch have

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 65 in the neighbouring lake Stevatn only grow to small sizes on fish or, rarely, a rich invertebrate resource. But some because Lepidurus is cropped down (Klemetsen et al., 1985). piscivores have evolved further, as indicated by a genetic Skulason et al. (1999) proposed a stepwise model influence on morphology in some cases. The commonly with four phases leading to speciation through resource observed segregation between littoral-benthic and pelagic based polymorphisms in fishes. The model is influenced morphs seems to have proceeded to a phase of clear by the theories of West-Eberhardt (1989, 2003, 2005) on genetic influence in some, but not all, cases. Reproductive developmental plasticity in sympatric evolution. The isolation by time and place of spawning in benthic–pelagic relative importance of phenotypic plasticity, genetics, pairs is found in some lakes but is less clear in others. and population segregation in controlling behaviour, There are therefore large variations among the many morphology and life history varies between phases, with charr polymorphisms that are now studied with respect phenotypic plasticity being most important in the first to how far the divergence has proceeded. This was phase and genetic basis in the third and fourth phase. The clearly demonstrated among Icelandic lakes by Gislason fourth phase is reproductive isolation (Skulason et al., 1999: et al. (1999) and is evident all over the distribution area of Table 4.3). Skulason et al. emphasised the great importance arctic charr (Snorrason & Skulason, 2004). Moreover, the of feeding behaviour in the formation of sympatric cases with three or four morphs show that there are clear morphs. Snorrason & Skulason (2004: Box 10.2) further differences also within lakes in how far the divergence elaborated a framework for the evolution of arctic charr has proceeded. In Thingvallavatn, the main segregation trophic polymorphisms. Here, the basic assumption is that is between the pelagic and benthic morphotypes but the postglacial freshwater systems develop more predictable further divergence is more pronounced between the food resources and habitats after an initial phase of benthic morphs, with the unique niche expansion of the instability. With time and increasing environmental small benthic charr to the hidden resources of the lava predictability, resource morphs can evolve from an originally surf zone, also found elsewhere in Iceland, than between monomorphic, but phenotypically plastic, population. the pelagic morphs. In Rannoch, the main divergence is With the right combination of ecological and intrinsic also between the pelagic and benthic morphs, although the factors, such morphs may proceed further to reproductive less studied piscivore may be genetically more segregated isolation and, eventually, speciation, becoming more and than in other cases. In Fjellfrøsvatn, the benthic–pelagic more specialised during the development. The theoretical divergence is in a very early phase, while the profundal contributions of Adams (1999), Skulason et al. (1999) and charr has proceeded far towards speciation. This also Snorrason & Skulason (2004), emphasising the ontogenetic seems to be the case for the advanced segregation of the type of development in the early, highly plastic phase, are profundal morph in Lake Davatchan (Alekseyev et al., all based on the long research effort on the charr problem 2002). As already pointed out by Frost (1965), separate as outlined in the present review, and fit well into the time and place of spawning is central in sympatric framework of natural selection and ecological speciation charr evolution. The clearest cases have no overlap in as discussed and defined by Rundle & Schluter (2004). spawning time, but spawning grounds may also be Most charr polymorphisms in the literature (see clearly separated in space, in which case site fidelity will Johnson, 1980; Jonsson & Jonsson, 2001; and Klemetsen be important. Transplantation experiments have shown et al., 2003), and the cases treated in detail in the present that lacustrine charr have high site fidelities (Frost, 1965; essay, fit into these models. Open, migratory systems Svenning & Grotnes, 1991). Adams et al. (2006) showed are in an early phase with high phenotypic plasticity that despite effective sympatry (no migration barriers) in intact, particularly with respect to life history strategies three lochs in the upper Forth catchment, the populations that influence growth and size heavily. This also seems were kept apart by site fidelity during spawning, resulting to be the case with morphs that grow large by feeding

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 66 Klemetsen, A. in functional allopatric divergence. Such traits are no Tinnsjøen. Controlled laboratory studies of the profundal doubt important if charr polymorphisms are to develop. morph from the much less deep Fjellfrøsvatn, have already The few cases we now know of permanent life at demonstrated genetically based traits (loss of spawning the bottom in deep water are dispersed all over the colour, specialised morphology and feeding behaviour, circumpolar distribution of S. alpinus (Siberia, Scandinavia, high growth potential on restricted food resources) Central Europe, and Canada) like the many cases of that most likely are adaptations to life in deep water. littoral benthic–pelagic polymorphisms. This shows that Most studies conclude that co-occurring populations sympatric divergence to deep water niches can occur of arctic charr are of sympatric origin (Skulason et al., anywhere given the right conditions. As with the benthic 1999; Jonsson & Jonsson, 2001; Snorrason & Skulason, littoral–pelagic pairs, the high degree of phenotypic 2004; Wilson et al., 2004). There are, however, possible plasticity in arctic charr forms the evolutionary basis, but exceptions to this. Wilson et al. (2004) found genetically there is an interesting and important difference: the deep distinct sympatric populations in 10 out of 43 lakes from water morphs definitely seem to have come further in their northern Europe by microsatellite DNA. Monophyletic evolution. Reproductive isolation is clearly documented grouping was supported in most cases except for Loch in well-studied cases and divergence has developed to an Rannoch (the text in the discussion of Wilson et al. refers to advanced, specialised and less plastic level, in many cases Loch Tay (p. 1137), but it is an error, as the actual population possibly to complete speciation. The profundal habitat studied was in Loch Rannoch in the Tay catchment (see of lakes is a special environment. It is always dark, the p. 1131); Alastair Wilson, personal communication) and temperatures vary little with season and year, and the Fjellfrøsvatn. Wilson et al. wrote that this could indicate sediments are flat, soft and without the vertical dimension an allopatric origin, with sympatry arising from repeated provided by plants and stones in the littoral. It is a refuge colonisation. Two other interesting cases were found in from predation because there are few piscivorous fish Loch Stack and Loch Maree, where only one population was and diving birds. But there is also little food, and that closely related to others in their respective lake catchments. is difficult to find because it is often hidden in the soft Based on the presence of an uncommon mtDNA variant sediment. Successful profundal life most likely depends in Loch Rannoch that also has been found in Hammerfest, on adaptation by natural selection to the special conditions, North Norway (Jonasson, 1987), Hartley et al. (1992) and above all the restricted food resources. Recent results from Volpe & Ferguson (1996) suggested a possible double studies of profundal morphs indicate that such evolution invasion of charr to Loch Rannoch. Postglacial invasion to has taken place (Alekseyev & Pichugin, 1998; Alekseyev et Europe from separate glacial refugia has been suggested al., 2002; Klemetsen et al., 2002a, 2006; Knudsen et al., 2006). for brown trout Salmo trutta L. (Ferguson & Taggart, 1991; Also, the endemic longfin charr Salvethymus svetovidovi Garcia-Marin et al., 1999), whitefishCoregonus (Bernatchez Chereshnev & Skopets from deep water in the very old & Dodson, 1994; Svärdson, 1998), perch Perca fluviatilis L. Lake Elgygytkyn (3.5 Myr to 4 Myr) in Chukotka, Russia (Refseth et al., 1998; Nesbø et al., 1999), and arctic charr (Chereshnev & Skopets, 1990) testifies that profundal (Klemetsen & Grotnes, 1980; Nyman et al., 1981; Hammar, evolution can yield unique and remarkable results. 1984); and for arctic charr to North America (McPhail, 1961; The enigmatic, very deep charr of Tinnsjøen and Wilson et al., 1996; Bernatchez et al., 1998). A geographic Gander Lake deserve further attention because their pattern of esterase frequencies suggested oppositely extreme environments must impose strong selective forces, directed invasions to northern Norway from refugia in as already indicated by the ploughing behaviour in the soft Siberia and south-west Europe (Klemetsen, 1991). Support sediments seen in video films from Gander and Tinnsjøen for this may be seen in the mtDNA study by Brunner et (possibly an adaptation to feeding on burrowing prey), and al. (2001) who found that Siberian and Atlantic lineages the dysfunctional eyes found in the first specimens from met in northern Fennoscandia. With more material from

© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3 Phenotypic plasticity leads to speciation in Arctic charr 67

Siberia, Alekseyev et al. (2009) later concluded that the also of all fishes, or even vertebrates; in geographic Atlantic and Siberian lineages were closely related and range, phenotype (colour, form, size, behaviour), ecology, should be considered as subgroups within one Eurasian life history and the expression of polymorphisms. In group. Alekseyev et al. also proposed that coastal Siberia vertebrates, high intraspecific variability is not to be was re-colonised in postglacial times from the west by expected in birds and mammals because of restraints this Eurasian group. Invasions from separate refugia imposed by their homoiothermic physiology. In fishes, to a lake would give rapid divergence because genetic the highest intraspecific variability is found in postglacial differences evolved during the glaciations might jump- waters, particularly in salmonids (the high variability in start the segregation. This could happen if charr from one tropical cichlids and other families is mostly among, not group invaded another group (e.g. Siberian to Atlantic), within, species). Fleming & Einum (in press) noted that and is the most likely explanation for the few cases where the variability in age and size at maturation of Atlantic a non-monophyletic origin is indicated. Moreover, an salmon is matched by few vertebrates. This is true for allopatric origin does not necessarily mean long time size (Arctic charr comes close) but the salmon does not segregation in glacial refugia. It can also imply a period match the extreme variation of the charr in all other of postglacial allopatry, followed by further colonisation respects, not the least the expression of polymorphisms. to new catchments or lakes, with or without the help of There is progress in contemporary research on the man. Hunter-gatherers invaded the postglacial landscapes charr problem. Important achievements have come by at about the same time as fish, and may well have helped concentrated effort on certain lakes followed by comparative charr across migration barriers a long time ago. Even a expansion to regions, by combining experiments and field short period of isolation can pre-adapt populations for work, by a shift of focus from structure to process, by co-existence, priming a rapid speciation (West-Eberhardt, employing new molecular genetics methods, and by fitting 1989). Rapid selection in allopatric arctic charr populations results into modern theory of developmental, phenotypic was recently demonstrated by Conejeros et al. (2008) by plasticity (West-Eberhardt, 2003, 2005), adaptive radiation analysing a major histocompatability gene polymorphism. (Schluter, 2000) and adaptive speciation (Dieckmann et al., In a paper to celebrate Darwin, Losos & Riclefs 2004). New progress is likely to be gained by continued (2009) discuss the controversy between contingency and testing of the theory of developmental plasticity on the determinism in evolution (starting with the famous claim charr problem, above all the challenge that there are by Gould (1989) that replay of the evolutionary tape would large variations in the manifestations of polymorphisms give a different outcome every time) and conclude that among and within lakes; by comparisons along carefully islands provide excellent examples of both contingent and selected gradients from high to low environmental deterministic evolutionary patterns, the latter not necessarily stability; by finding possible rare cases of double invasions, in phenotype but often in the shape of functional niche preferably across geographic lineages, to test if pre- filling (Conway Morris, 2003). Postglacial lakes, viewed adaptations prime an accelerated start to the evolution of as inverted islands, demonstrate the same, with the many alternative resource phenotypes; by further testing of the repeated cases of deterministic, parallel benthic–pelagic notion that trophic behaviour provides the first response polymorphisms, but also with more contingent cases like to natural selection; by following up the importance the two planktivores in Windermere, the lava intruder of heterochrony in morphological development; by in Thingvallavatn and the deep water niche expander in looking more closely at the relation between genetic and Fjellfrøsvatn. Northern lakes with arctic charr provide ontogenetic development of piscivores (cannibals); and excellent opportunities to further study this contradiction. by studying more closely the contingent cases of morph Arctic charr is now beyond doubt established as the expressions, particularly the recently discovered very most variable of all postglacial fishes and most probably deep profundal morphs because of the probability that

DOI: 10.1608/FRJ-3.1.3 Freshwater Reviews (2010) 3, pp. 49-74 68 Klemetsen, A. strong selective forces operate in their environments. So, Ireland – 15 species or one? Ecology of Freshwater Fish 16, 20-28. the charr problem is still with us and will, fortunately, Adams, C.E., Fraser, D., Huntingford, F.A., Greer, R., Askew, C.M. continue to pose questions about the evolutionary play & Walker, A. (1998). Trophic polymorphism amongst arctic in the ecological theatre of northern postglacial lakes. charr from Loch Rannoch, Scotland. Journal of Fish Biology 52, 1259-1271. Acknowledgements Adams, C.E., Hamilton, D.J., McCarthy, I., Wilson, A.J., Grant, G., Waldron, S., Snorrason, S.S., Ferguson, M.M. & Skulason, I am grateful to Colin Reynolds for inviting me to write S. (2006). Does breeding site fidelity drive phenotypic and this review and to my colleagues Per-Arne Amundsen genotypic sub-structuring in a population of arctic charr? and Rune Knudsen for their comments to the manuscript Evolutionary Ecology 20, 11-26. before submission. Colin Reynolds and two referees Adams, C.E., Fraser, D., Wilson, A.J., Alexander, G., Ferguson, gave very encouraging and constructive comments to the M.M. & Skulason, S. (2007). Patterns of phenotypic and genetic submitted manuscript. Martin Svenning kindly permitted variability show hidden diversity in Scottish arctic charr. Ecology reprinting of Fig. 1 and Colin Adams kindly permitted of Freshwater Fish 16, 78-86. reprinting of the modified Fig. 5. I also thank Malcolm Adams, C.E., Wilson, A.J. & Ferguson, M.M. (2008). Parallel Elliott for providing the photo of Winifred Frost from the divergence of sympatric genetic and body size forms of arctic FBA Collection (Fig. 2), Rune Knudsen for the photos of the charr, Salvelinus alpinus, from two Scottish lakes. Biological Fjellfrøsvatn charr (Fig. 3), Fredrik Søreide for the photo of Journal of the Linnean Society 95, 748-757. the deep-living charr in Tinnsjøen (Fig. 4), Frøydis Strand Alekseyev, S.S. & Pichugin, M.Y. (1998). A new form of charr, for drawing Fig. 5, and Synnøve des Bouvrie for finding Salvelinus alpinus (Salmonidae) from Lake Davatchan in the correct Latin for life in the deep. Transbaikalia and its morphological differences from sympatric This contribution is dedicated to Per Grotnes; friend, forms. Journal of Ichthyology 38, 292-302. colleague and a source of great inspiration for research Alekseyev, S.S., Samusenok, V.P., Matveev, A.N. & Pichugin, on charr ecology and evolution through many years. M.Y. (2002). Diversification, sympatric speciation, and trophic polymorphism of arctic charr Salvelinus alpinus complex, in References Transbaikalia. Environmental Biology of Fishes 64, 97-114. Alekseyev, S.S., Bajno, R., Gordeeva, N.V., Reist, J.D., Power, Adams, C.E. (1999). Does the underlying nature of polymorphism M., Kirillov, A.F., Samusenok, V.P. & Matveev, A.N. (2009). in the arctic charr differ across the species? International Society Phylogeography and sympatric differentiation of the arctic of Arctic Char Fanatics Information Series 7, 61-67. charr Salvelinus alpinus (L.) complex in Siberia as revealed by Adams, C.E. & Huntingford, F.A. (2002a). Inherited differences in mtDNA sequence analysis. Journal of Fish Biology 75, 368-392. head allometry in polymorphic arctic charr from Loch Rannoch, Amundsen, P.-A., Svenning, M.-A. & Siikavuopio, S.I. (1999). An Scotland. Journal of Fish Biology 60, 515-520. experimental comparison of cannibalistic response in different Adams, C.E. & Huntingford, F.A. (2002b). The functional arctic charr (Salvelinus alpinus (L.)) stocks. Ecology of Freshwater significance of inherited differences in feeding morphology in Fish 8, 43-48. a polymorphic population of arctic charr. Evolutionary Ecology Amundsen, P.-A., Knudsen, R. & Klemetsen, A. (2008). Seasonal 16, 15-25. and ontogenetic variations in resource use of two sympatric Adams, C.E. & Huntingford, F.A. (2004). Incipient speciation arctic charr morphs. Environmental Biology of Fishes 83, 45-56. driven by phenotypic plasticity? Evidence from sympatric Balon, E.K. & Penczak, T. (1980). The dwarfed charr of Dösener populations of arctic charr. Biological Journal of the Linnean See, an alpine lake in Austria. In: Charrs, Salmonid Fishes of the Society 81, 611-618. Genus Salvelinus (ed. E.K. Balon), pp. 773-796. W. Junk, The Adams, C.E. & Maitland, P.S. (2007). Arctic charr in Britain and Hague.

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© Freshwater Biological Association 2010 DOI: 10.1608/FRJ-3.1.3