Ecological polymorphism in Arctic charr

Biological Journal of the Linnean Society (1993), 48: 63-74. With 3 figures

Ecological polymorphism in Arctic charr KJETIL HINDAR AND BROR JONSSON Norwegian Institute for Nature Research, Tungasletta 2, N-700.5 Trondheim, Norway Received 22 M a y 1991, accepted for publication 26 September 1991

Arctic charr, Salvelinus alpinus (L.), commonly exhibits two coexisting morphotypes, dwarf and normal charr, which are characterized by differences in adult body size and colouration. We tested whethei or not the morphotypic differences were genetically determined in rearing experiments with offspring of the two morphs and of their crosses. The experiments suggest that this ecological polymorphism in Arctic charr is largely environmentally determined. When reared under similar conditions, offspring of each of the two morphs differed little in size at the same age, and they had the same early developmental rate and maturation pattern. Moreover, the presence of parr marks along the flanks of the fish, one characteristic of dwarf charr, depended on body size and not on parental morph. Genetic differences between the morphs were suggested for growth rate during the second year of life, and for jaw morphology. Comparisons between charr life histories in captivity and in the wild suggest that ecological polymorphism in Arctic charr is chiefly a result of variation in growth conditions between different habitats.

KEY WORDS:-Morphotype

-

intrapopulation variation

-

rearing study

-

Salvelinus alpinus

-

Salmonidae. CONTENTS Introduction . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . Source population Experimental matings . . . . . . . . . Characters studied . . . . . . . . . . Results . . . . . . . . . . . . . . . Development and mortality . . . . . . . . Size at the same age . . . . . . . . . . Sexual maturation . . . . . . . . . . Parr marks and jaw length . . . . . . . . Comparison with the natural population . . . . . Discussion . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . References . . . . . . . . . . . . .

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63 64 64 64 65 66 66 67 68 68 68 70 72 73

INTRODUCTION

A central problem of evolutionary biology is whether a single population contains one or more optimum phenotypes (Ludwig, 1950; Van Valen, 1965; Wilson, 1989). Polymorphism in ecological or morphological traits has frequently been misinterpreted as speciation, due to lack of knowledge about the range and nature of phenotypic variation within populations (Sage & Selander, 1975). Certainly, there are well-known cases where the morphs represent 0024-4066/93/010063

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0 1993 The Linnean

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K. HINDAR AND B. JONSSON

separate evolutionary lineages that should be classified as different species (e.g. several Old World cichlids; McKaye et al., 1984; Meyer et al., 1990), but it has also been shown that equally large phenotypic variation can occur within a single gene pool. Examples of such intrapopulation polymorphisms include the trophic morphology of fishes (Sage & Selander, 1975; Turner & Grosse, 1980; Kornfield et al., 1982) and birds (Smith, 1987), and body morphology and behaviour of fishes (Savvaitova, 1973; Hindar & Jonsson, 1982; Nordeng, 1983; Gross, 1984; Jonsson, 1985, 1989; Ehlinger & Wilson, 1988) and insects (Roff, 1986). In a few cases, a simple genetic basis for the phenotypic polymorphism has been documented (e.g. Zimmerer & Kallman, 1989); in most instances, however, it is not known what roles are played by genetic and environmental variation in producing the different phenotypes. At least three hypotheses may explain how polymorphisms in morphological or ecological traits are maintained: (1) the morphs belong to separate gene pools, (2) they belong to a single gene pool in which the polymorphism is genetically determined, and (3) they are produced by environmental variation acting on a single gene pool through conditional development. I n the present study, we examined to what extent these hypotheses could account for the coexistence of ‘dwarf and ‘normal’-sized morphotypes of Arctic charr, Salvelinus alpinus (L.); a widespread morphological and ecological polymorphism which has led to much taxonomic conjecture (e.g. Reisinger, 1953; Behnke, 1972; Nyman, 1972; Johnson, 1980; Nyman, Hammar & Gydemo, 1981; Nordeng, 1983; Hindar, Ryman & StHhl, 1986; Jonsson et al., 1988; Svedang, 1990). Here we test whether or not dwarf and normal Arctic charr maintain the morphological and ecological polymorphism when reared under the same experimental conditions. If the morphological and ecological differences between the morphs are genetically determined, we would expect that the experimentally reared offspring would differ in size at the same age, age a t sexual maturity, colouration and jaw morphology. If, however, the phenotypic polymorphism is produced by environmental variation, the reared offspring of the two morphs should develop at the same rate and become indistinguishable as adults. METHODS

Source population We used Arctic charr from Lake Vangsvatnet, western Norway, where dwarf and normal charr mature at the same ages and are found in both sexes (Hindar & Jonsson, 1982; Jonsson & Hindar, 1982). Dwarf charr have an adult body length of 140-270 mm (Fig. l ) , overshot (sub-terminal) mouth and dull spawning colours with parr marks along the flanks. T h e faster-growing normal charr are 180-430 mm in adult body length, have a terminal mouth, and bright spawning colours without visible parr marks. The two morphs overlap in spawning time and place, but dwarfs breed on average at greater depths and later in the season than normals.

Experimental matings We crossed eggs and sperm from dwarf and normal Arctic charr sampled a t the same spawning site in Lake Vangsvatnet during two consecutive years.

SYMPATRIC MORPHOTYPES OF SALVELINUS ALPINUS

65

12

--8 10 s

8 6 e,

LL

4 2 0 I50

250

350

Fish length (rnm)

Figure 1 . Length distributions of sexually mature Arctic charr ( N = 865) in Lake Vangsvatnet, western Norway, 1977-81. Filled and open columns designate respectively dwarf charr and normal charr. (Modified from Jonsson & Hindar, 1982.)

Gametes were pooled from 10-40 charr of each sex and morph to produce: ( 1 ) two pure-morph strains (N x N, normal females x normal males; and D x D, dwarf females x dwarf males) within the 1984 year class, and (2) two puremorph strains ( N x N, D x D) and two reciprocal hybrid-morph strains (N x D, D x N) within the 1985 year class. The two strains of the 1984 year class were incubated at elevated temperatures and later reared in 4 m2 outdoor tanks for two years at the ambient temperatures of the River Imsa (cf. Jonsson, Jonsson & Ruud-Hansen, 1988). The four strains of the 1985 year class were both incubated and reared a t ambient temperatures. Within both year classes, the fish were fed to satiation on dry pellet food (Ewos). We reared the different strains in separate tanks during the first year and in a common tank (after group marking by fin-clipping) during the second year. All remaining fish of the two year classes were killed at the end of their second year.

Characters studied Developmental times were registered as the number of days from fertilization to the first appearance of eyed eggs and hatching, respectively. Natural tip lengths (Ricker, 1979; 1 mm precision) were measured once a year in late October-early November when the fish were inspected for sexual maturity. Mortality was registered daily. For the 1984 year class, we examined the fish for presence or absence of parr marks and measured the lengths of the upper and lower jaws with a caliper (0.1 mm precision) in July of the second year. Mortality rates during the first year of life (300 days, 10-day intervals) were compared using the Kruskal-Wallis test (Sokal & Rohlf, 1981). Fish lengths were compared by using one- or two-way analysis of variance, following the ANOVA procedure of Norusis (1986). The two year classes were analysed separately because rearing conditions differed between years. Differences in the proportion of fish with parr marks were tested by using the normal approximation to the binomial distribution (Siegel, 1956).

66


RESULTS

Development and mortality Early development was faster in the 1984 year class than in the 1985 year class due to elevated incubation temperatures in the former. I n the 1984 year class, the first eyed eggs appeared after 28 days and hatching started after 58 days. In the 1985 year class, the corresponding developmental times were 49 and 104 days, respectively. Within year classes, all strains developed at the same rate and had identical dates for the first appearance of eyed eggs and hatching. Mortality rates during the first 300-day period following fertilization were very high ( > 90%) in both the 1984 and the 1985 year classes. This was probably due to imperfect rearing techniques, as most of this mortality occurred during the start-feeding period (we noted a slight improvement in the 1985 year class, which experienced lower temperatures during incubation and startfeeding). Within the 1984 year class, the mortality pattern over the first 300-day period did not differ between the two pure-morph strains (Kruskal-Wallis test statistic, H = 0.79, d.f. = 1, P > 0.25). Within the 1985 year class, however, the mortality pattern was heterogeneous among strains ( H = 15.17, d.f. = 3, P < 0.01). Mortality rates between the end of the first and second growing seasons (cf. Table 1 ) were lower than during the first 300-day period. Within the 1984 year class, the two pure-morph strains both had a mortality of about 10% during the second year of life. Within the 1985 year class, the mortality varied from 4% in the dwarf strain to 31% in the normal strain and more than 50% in the two hybrid-morph strains, and was highly significant among strains (x' = 56.02, d.f. = 3, P < 0.001).

TABLE 1. Natural tip length (averagefstandard deviation, mm) of offspring of dwarf and normal Arctic charr at age 0' and l', and relative length increase during the second year of life. (Numbers in parentheses represent all remaining fish at the time of sampling) 1984 year class Cross (Male x female)

A, At age O+ Normal x normal Dwarfx dwarf Normal x dwarf Dwarfx normal

Immature

Mature

126f 19(83) 124f 19(74)

1985 year class Immature

Mature

87 f20(246) 96 f20( 121) 82f18 (16) 91f21 (39)

B, At age 1 + Normal x normal Dwarfx dwarf Normal x dwarf Dwarfx normal

202 f32(20) 180 f42( 18)

C, Per cent length increase from age O + to age I + Normal x normal 60 Dwarfx dwarf 45 Normal x dwarf Dwarfx normal

243f24(56) 223f22(48)

93 80

161 f 3 6 (63) 152f16 (31) 147f19 (5) 168f30 (7) 85 58 79 85

217 f 3 0 ( 107) 210f31 (85) 185f 6 (2) 215f20 ( 1 1 ) 149 119 126 136


67

Fish length lrnrn)

Figure 2. Length distributions of offspring of dwarf charr (---), normal charr (-) and of crosses between the two (-. .-) at the end of the second growing season (age 1 '). A, 1984 year class; B, 1985 year class.

Size at the same age Average fish lengths were larger in the 1984 year class than in the 1985 year class, both at the end of the first (age 0') and second (age 1 +) year (Table lA, B). Within year classes, large overlap was observed in the length distributions of pure-morph and hybrid-morph strains (Fig. 2). For the 1984 year class, analysis of variance of length showed no significant difference between strains at age O+, but did so at age 1' when the normal charr strain was the larger (Table 2). For the 1985 year class, there were significant strain differences in length a t age O+ when the dwarf charr strain was the largest, but not a t age 1 +. For both year classes, significant length differences existed between sexually mature and immature fish at age 1 +. Sexually mature fish were larger than immature fish in all comparisons, or, in other words, there was no significant interaction between strain and maturity stage in the two-way analyses (Table 2). The sample sizes of

TABLE 2. Analysis of variance for natural tip length of offspring of dwarf (D) and normal (N) Arctic charr in rearing experiments 1985 year class (NxN, DxD, NxD, DxN)

1984 year class (NxN,DxD)

SSQ

MS

Source of variation

d.f.

A, At age ' 0 Strain Residual

155

237 55 347

237 357

Total

I56

55 584

356

1

1

B, At age 1' Strain Maturity stage Strain x maturity stage Residual

1 I38

14 131 49 545 16 103 843

Total

141

168 113

1

F 0.66"$

14 131 18.78*** 49545 65.84*** 16 0.02" 752 1192

d.f.

SSQ

3 418

8475 169 117

2825 405

42 I

177592

422

3 3 303

5957 208 882 873 275810

310

495 530

1

MS

F 6.98***

1986 2.18" 208882 229.47*** 291 0.32" 910 1598

Abbreviations: SSQ sum of squares; MS, mean square; F, variance ratio; "kot significant; * * * P < 0.001.

68

K. HINDAR AND B.JONSSON

the N x D and D x N strains are small in these analyses; however, lumping of these two groups into one hybrid-morph strain did not give qualitatively different results. The average growth rate during the second year of life, calculated from the average lengths at age 0' and age 1' (Table l C ) , showed more consistent differences between strains. The proportionate size increase of the dwarf charr strain was less than that of the normal strain in both year classes, and in both sexually mature and immature individuals. Furthermore, the proportionate size increases of the two hybrid-morph strains were intermediate between those of the two pure-morph strains. In the absence of individually marked fish, these growth-rate differences were not subjected to statistical analysis.

Sexual maturation No fish matured sexually at age '0 in either year class. At age 1 +,73% of the 1984 year class and 66% of the 1985 year class were sexually mature. The proportion of sexually mature individuals did not differ between strains within the 1984 year class (x' = 0.02, d.f. = 1, P > 0.75). In the 1985 year class, there was a marginally significant heterogeneity in age at sexual maturity (x' = 8.00, d.f. = 3, P < 0.05). This was due to a majority of N x D hybrids still being immature (five out of seven individuals), whereas most individuals within the three other strains were sexually mature (Table 1).

Parr marks andjaw length The two pure-morph strains could not be distinguished on the basis of presence or absence of parr marks. The disappearance of the parr marks was connected to size: the smallest fish without parr marks were 160 mm and no fish larger than 240 mm showed parr marks along the flanks (Fig. 3). Within this length interval, normal and dwarf charr strains did not lose their parr marks at different lengths ( 0.10). Both pure-morph strains had overshot mouths. The difference between the lengths of the upper and lower maxillary bones ( U - L, mm) was for dwarf and normal charr strains equal to 1.18f0.69 mm and 0.86f0.71 mm (average fstandard deviation), respectively. Tested with analysis of variance and correcting for fish length by dividing with the sum of the lengths of the upper and lower maxillary bones ( ( U - L )/ (U+ L ) , mm), this difference was = 6.83, P < 0.01). significant (F,,,52

Cornbarison with the natural population Native Arctic charr in Lake Vangsvatnet commonly do not mature until age 4' or 5 + , when respectively 28% and 73% of the fish are sexually mature (Jonsson & Hindar, 1982). At this age (e.g. 4 + ) , there are highly significant differences in length between dwarf and normal charr morphotypes (classified by their colouration) and between sexually mature fish and immature ones (Table 3). But unlike in the rearing experiments, there is significant interaction between morphotype and maturity stage at age 4' in Lake Vangsvatnet, resulting from there being no difference in average length of sexually mature and

SYMPATRIC MORPHOTYPES O F SALVELINUS ALPINUS

69

c

0

n tl

5 30

I60

200

180

220

240

Fish length ( m m )

Figure 3. Occurrence of parr marks among offspring of dwarf and normal Arctic charr in rearing experiments (1984 year class). Filled and open columns designate respectively presence or absence of parr marks. A, Normal charr strain; B, Dwarf charr strain.

immature dwarf charr (196 vs 198 mm) whereas sexually mature normal charr were significantly larger than their immature counterparts (272 vs 261 mm). The absolute difference in average length (1 1 mm) between mature and immature normal charr in Lake Vangsvatnet is only about one-fourth of that in TABLE 3. Analysis of variance for natural tip length of dwarf and normal Arctic charr at age 4' from Lake Vangsvatnet, October 1977-March 1978 Source of variation

d.f.

SSQ

MS

F

Morphotype Maturity stage Morphotype x maturity stage Residual

1 1 1 628

275 207 10 224 2053 330 958

275 207 10224 2053 527

522.21*** 19.40*** 3.90;

Total

63 1

61 I648

969

Abbreviations: SSQ, sum of squares; MS, mean square; F, variance ratio; * P < 0.05; ***P < 0.001.

70


similar comparisons in the rearing experiments (Table 1). O n the other hand, the absolute difference in average length of normal and dwarf charr at age 4' in the lake (264 vs 197 mm), is two to several times larger than the differences between strains in the rearing experiments. DISCUSSION

The mechanisms underlying the coexistence of dwarf and normal Arctic charr have been a matter of considerable debate. One set of questions relates to the degree of reproductive isolation between the different morphotypes, and ultimately, whether or not they represent different evolutionary lineages. I n the present study, we observed a higher mortality of hybrid-morph than pure-morph strains during the second year of life. If this occurs in the wild, it could reinforce possible assortative mating among dwarf and normal charr (Jonsson & Hindar, 1982) and lead to partial reproductive isolation between them. But the variation in mortality in the common tank could also be explained by size-dependent mortality acting more strongly on small fish, since the lowest mortality was found among the dwarf strain which was the largest at age 0' (cf. Table 1). In a multiple-locus electrophoretic study of sympatric morphotypes from several geographically isolated lakes, Hindar el al. (1986) concluded that dwarf and normal Arctic charr are conspecific, and that they even appear to belong to the same breeding population in some lakes, including Lake Vangsvatnet. So far, the combined ecological and genetic evidence suggests that dwarf and normal charr in this lake are not reproductively isolated (Jonsson & Hindar, 1982; Hindar et al., 1986). Another set of questions relates to how genetic and environmental factors influence the various polymorphic traits that characterize dwarf and normal charr in the wild. This was addressed by the present study for both performance traits (early developmental rate, mortality, size at the same age, and age at sexual maturity) and morphological traits (colouration and jaw morphology). When reared under similar conditions offspring of dwarf and normal charr and of their crosses had the same early developmental rate, and they showed small or no differences in size at the same age and age a t maturity. Moreover, all strains showed the same maturation strategy in the rearing experiments as do normal charr-but not dwarf charr-in nature; namely, that individuals maturing sexually were larger than immature individuals of the same age. The presence of parr marks, one morphological characteristic of dwarf charr in nature, was related to the size of the fish and not to the parental morphotype. The loss of parr marks occurred within the same length interval in our rearing study (160-240 mm) as in the source population in Lake Vangsvatnet (150-250 mm, Hindar & Jonsson, 1982). Thus, all strains showed the same transition from the morphological characteristics of the parr stage to those attained by normal charr in Lake Vangsvatnet when they change from benthic to pelagic living. It is unlikely that the similarities between strains in both performance and morphological traits are artefacts caused by the rearing environment. The 1984 and 1985 year classes experienced different rearing conditions, resulting in variation between year classes in growth and survival. Nevertheless, offspring of the two morphotypes were quite similar within each year class. The capability


71

of the dwarf charr strain to develop as normal charr in this rearing study rejects the hypothesis of genetic determination of dwarf charr traits, which is implicit in the classification of dwarf charr into one or more species showing diagnostic differences from normal charr in traits such as growth rate and size at maturity in sympatry (Nyman, 1972; Nyman et al., 1981). Even though there appears to be a large environmental component to most traits that distinguish between dwarf and normal Arctic charr in the wild, some underlying genetic differences between the morphotypes are also apparent in this rearing study. The normal charr strain showed a consistently higher growth rate than the dwarf charr strain during the second year of life, with the hybrid-morph strains showing an intermediate position. This probably reflects genetic differences in growth rate between the morphotypes. Another genetic difference found between offspring of dwarf and normal charr in our experiments was that the former had a more overshot mouth than the latter. These differences may reflect that the morphotypes live and feed in those habitats of Lake Vangsvatnet to which they are best adapted. Our study does not test to what extent habitat choice is influenced by parental morphotype, but Nordeng’s (1983) rearing and release experiments with offspring of freshwater resident and anadromous Arctic charr suggest that the habitat choice is less dependent on parental morph than on growth rate and age at sexual maturity. Why do Arctic charr that belong to a single natural population develop into both dwarf and normal morphotypes? Nothing in our data suggests that this polymorphism can be attributed to genetic variation a t a single, diallelic locus, as has been implied for some other species (Dominey, 1980; Smith, 1987). Rather, the polymorphism appears to be a threshold trait with polygenic inheritance, where environmentally induced variation in growth rate plays a larger role for expression of the dwarf or normal phenotype than does genetic background. Fish typically show larger phenotypic variation and lower heritabilities for traits such as growth rate than other vertebrates, indicating greater susceptibility to environmental factors (Allendorf, Ryman & Utter, 1987; Weatherley & Gill, 1987: 3-8). The observed growth differences between dwarf and normal charr in Lake Vangsvatnet could therefore be caused by differences in food supply between their habitats. But this does not explain why some charr mature as dwarfs instead of delaying sexual maturity for one or more years to increase adult size. We believe the solution to this problem lies in the observation that vital aspects of salmonid life histories (e.g. age and size at smolting and maturity) are finely tuned to growth-rate variation (Nordeng, 1983; Jonsson, 1989). Maturation as dwarfs probably reflects the best option for individuals experiencing a slow growth rate, whereas maturation as normal charr is better for faster-growing individuals (Jonsson & Hindar, 1982). A change in morphotype has been observed for individuals which experience good growing conditions after having spawned as dwarf charr, clearly demonstrating the conditional nature of the dwarf trait (Nordeng, 1983). This conditional strategy (Maynard Smith, 1982: 78; Gross, 1984), in which individual tactics are determined by the size or dominance rank at specific life stages (Metcalfe et al., 1989; Gross, 1991), permits great flexibility of life histories with no or little genetic variation. As suggested by this study, some genetic variation probably exists, for example with respect to the interrelationship between growth rate and

72


threshold size for adopting the different individual tactics. It remains an open question whether fish maturing as dwarfs have lower fitness than faster-growing individuals maturing as normal charr. The evidence available to us suggests that dwarf charr do have lower fitness than normal charr in Lake Vangsvatnet (Jonsson & Hindar, 1982), whereas Gross (1985) suggested that two differentsized morphotypes of male coho salmon, Oncorhynchus kisutch (Walbaum), had equal fitnesses; the higher breeding success of one being compensated for by the higher survival of the other. The relative importance of the factors accounting for individual variation in growth rate is poorly known. These may include maternal effects, random food intake, random spacing, habitat heterogeneity and genetic variation for growth or habitat choice (Lomnicki, 1988). I n addition, social interactions may magnify initial size differences within a year class and lead to increased growth variation over time (Rubenstein, 1981; Jobling & Wandsvik, 1983; Metcalfe et al., 1989). Maternal effects may be more important under natural conditions than in our rearing study, as dwarf charr have smaller eggs than normal charr (Jonsson & Hindar, 1982), and larvae emerging from small eggs tend to be smaller than those emerging from large eggs (Kazakov, 1981). However, the size advantage shown by start-feeding fry from large eggs needs not be maintained during the first year of life (Thorpe, Miles & Keay, 1984). Moreover, back-calculation of length from otoliths of Arctic charr from Lake Vangsvatnet suggests that growth rate in the late parr stage (i.e. age group 2 + ) also influences adult size, especially among females (Jonsson & Hindar, 1982). The present rearing study suggests that genetic factors contribute to this growth variation. Coexisting morphotypes of Arctic charr may show larger genetic differences than in Lake Vangsvatnet, either as estimated from biochemically detected loci (Hindar et al., 1986) or from development of trophic morphology, growth rate, and size and age at sexual maturity in rearing experiments (Skulason, Noakes & Snorrason, 1989; Svedang, 1990). However, the amount of genetic differentiation between the coexisting morphotypes is generally smaller than between Arctic charr spawning in different localities. This pattern seems to hold true for parallel morphotypic variation in a number of salmonid fishes (Hindar et al., 1991), and may reflect that salmonid fishes adapt to heterogeneous environments (e.g. deep lakes or various combinations of river-lakeocean) by ecological polymorphism rather than by genetic population differentiation. At any rate, the available evidence from rearing or other genetic studies (Andersson, Ryman & Stbhl, 1983; Hindar et al., 1986) does not support the contention that coexisting Arctic charr morphotypes represent a complex of several species. ACKNOWLEDGEMENTS

We thank Nina Jonsson for help in the field, Jon G. Backer and the staff a t the Research Station for Freshwater Fish at Ims for rearing the fish, Steinar Engen for statistical advice, Finn Bkland for drawing the figures, Veronica Phillips Olsen for correcting the English, and Torbjorn Jarvi, Nils Ryman, Odd Terje Sandlund and an anonymous referee for comments on the manuscript. The Norwegian Institute for Nature Research and the Norwegian Fisheries Research Council provided financial support.

SYMPATRIC MORPHOTYPES OF S A L V E L I N U S A L P I N U S

73

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