The charr problem revisited: exceptional phenotypic plasticity ...

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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.

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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 et al., 2006). Later, Richardson (1836) established a new genus, Salvelinus, for the charrs.

Salvelinus alpinus (L.) is particularly difficult.

It

has a bewildering phenotypic and ecological diversity throughout its circumpolar range, and shows extreme

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

Fig. 1. The Arctic charr has a wide circumpolar distribution and 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

of the charr problem but also to the general discussion on ecologically driven speciation. By this treatment, much of

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Phenotypic plasticity leads to speciation in Arctic charr

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).

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.

About a hundred years later, Pennant

the polymorphisms are so frequent and, in some respects, spectacular and unique, that a special term is coined for charr but not for other postglacial fishes. Nordeng (1983)

Winifred E. Frost and the 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.

(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.

different sizes.

Windermere (Frost, 1951, 1963, 1965) was the first clear

She found that Windermere had separate

Her work on

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.

paper. This was a bold discussion at a time when Mayr’s

Later, he restricted the

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

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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 House, FBA Windermere Laboratory, was a pioneer in charr research. Her 1965 paper will always stand as a classic study on the charr problem. Photo from FBA Collection.

high.

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.

The spawning colours were also very similar,

perhaps with spring spawning males being a bit brighter. There was a significant difference in the mean number

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.

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.

The strong

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

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Phenotypic plasticity leads to speciation in Arctic charr

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

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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

fish

community

(Elliott

a

diverse

changing

their prey (Snorrason et al., 1989, 1994). The two benthic

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

et

al.,

and 1996;

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

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Phenotypic plasticity leads to speciation in Arctic charr

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 & Ferguson, 1987) and mtDNA (Danzmann et al., 1991) failed

had

genetic

components

that

differed

between

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.

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.

Inspired by the

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 Loch Rannoch, Scotland

Klemetsen, A.

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,

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).

© Freshwater Biological Association 2010

and

polymorphisms

were

disclosed

in

Together,

DOI: 10.1608/FRJ-3.1.3

57

Phenotypic plasticity leads to speciation in Arctic charr

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 and littoral benthos while the profundal morph feeds on

Fjellfrøsvatn, Norway

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 much larger than their wild parents (Fig. 3, lower panel). The study concluded that the differences between the Fjellfrøsvatn morphs in morphometry and growth capacity had a genetic basis. For the profundal charr, the better growth capacity may be an adaptation to restricted food resources. At maturity, offspring of the profundal morph had pale spawning colours like the wild parents (Fig. 3) while offspring of the littoral morph became very brightly coloured on the same food. This indicates that the cryptic DOI: 10.1608/FRJ-3.1.3

Fig 3. The subarctic lake Fjellfrøsvatn, Norway, has two reproductively isolated arctic charr morphs, termed littoral charr and profundal charr after their spawning places. Littoral charr spawn in shallow water in the autumn while profundal charr spawn in deep water five months later, under thick ice and snow. Genetic differences are found by microsatellite analysis, and also in morphology and behaviour. Upper panel: females and males of both morphs in spawning colours. Lower panel: mother and son; demonstrating the surprisingly high capacity for growth that profundal charr showed when given enough food in the laboratory. The son had pale spawning colours like the mother. The high capacity for growth and the pale spawning dress are probably genetic traits selected for in the profundal environment. Photos by Rune Knudsen. 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

origin.

gas even when given an opportunity to decompress at 5

The littoral morph has ontogenetic and seasonal

may

not

have

a

monophyletic

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

59

Phenotypic plasticity leads to speciation in Arctic charr

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.

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

Reproductive isolation

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).

Profundis vivens

The pneumatic ducts were probably

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 km ) 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

2

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 the deepest ever recorded for arctic charr at the time. The new and extensive material confirmed the differences in diet. Pale charr had a dominance of chironomid larvae in their stomachs, particularly in fishes caught in very deep DOI: 10.1608/FRJ-3.1.3

Fig. 4. An unknown charr, possibly a new profundal morph, was recently discovered at 400–450 m depths in Tinnsjøen, county Telemark, Norway. Tinnsjøen is one of very few lakes worldwide that are deeper than 400 m. This photograph was taken by a Remotely Operated Vessel ROV in 2004. The fishes were small, almost colourless and somewhat burrowed in the sediments. Two live specimens were brought to the surface by another ROV search in 2005. Photo by Fredrik Søreide. 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.

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

Meristic

are small-sized and pale, even when sexually mature, © Freshwater Biological Association 2010

DOI: 10.1608/FRJ-3.1.3

63

Phenotypic plasticity leads to speciation in Arctic charr

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.

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

Nordeng’s contribution now stands

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).

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

This means that individual fish can change

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

have adapted.

differences in food and growth. Piscivorous morphs are

Important progress has been achieved since Frost’s pioneering work.

mechanisms,

and

often

found in Thingvallavatn, Loch Rannoch and several other

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

65

Phenotypic plasticity leads to speciation in Arctic charr

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.

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.

This was

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), whitefish Coregonus (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

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Author Profile Anders Klemetsen is an emeritus Professor at the University of Tromsø, Norway. His main research interests include the ecology of freshwater and anadromous fish, trophic ecology, evolution in postglacial lakes, and freshwater invertebrates. He served on The Council of Freshwater Biological Association 2001-2004. At present he is member of the Board of The Nordic Society of Ecology Oikos and Chairman of the Board of The Oikos Editorial Office. DOI: 10.1608/FRJ-3.1.3