Genetic Contro e Life History Pattern in Chinook Sa

W. Craig Clarke, Ruth E. Withier, and john E. Shelbourn Department sf Fisheries and Oceans, Biological Sciences Branch, Pacific Biological Station, Nanaimo, 5.C. V9R 5K6, Canada

Clarke, W. C., R. E. Withler, and 1 . E. Shelbourn. 1992. Genetic control of juvenile life history pattern in chinook salmon (Oncsrkeynch~~s tshawytscha), Can. I. Fish. Aquat. Sci. 49: 2300-2306.

Ts investigate the genetic basis for the difference in photoperiod responses between juvenile ocean-type and stream-type chinook salmon (Osacorhynchus bhawytscha), we conducted two crossing experiments and exposed the progeny to either a short- sr long-day photoperiod for 10 wk from the time sf first feeding. The first experiment exami wed the photoperiod response sf pure and reciprocal crosses among red- and white-fleshed Quesne6 River (stream-type) chinook sal mon. The second experiment tested the photoperiod response of pure and reciprocal crosses between Quesnei River (stream-type) and Conuma River (ocean-type) chinook salmon. In both experi- ments, Qadesnel chinook salmon fry (both red and white fleshed) sustained a high growth rate and developed a high degree of seawater adaptability only when exposed first ts a short-day photoperiod for 18 wk and then to a Bong-day photoperiod. In contrast, the Conuma River chinook salmon grew rapidly and developed the increased seawater adaptability characteristic sf srnolts when reared on either photoperiod regime. Reciprocal Conuma- Quesnel hybrids displayed the ocean-type pattern of development, indicating that the photoperiod-independent phenotype i s dominant and not under maternal control.

Afin d'etudier les fondements genktiques des diff&-ences sur le plan de la reaction 2 [a photoperiode observ6es entre le jeune saumon quiwnat (Oncoshynchus &hawy&c%la) des oceans et celui des cours d'eau, nous avons effectu6 des experiences de croisement et avons expose la progeniture 2 une photsperide 2 phase diurne lsngue ou courte pendant 10 sern 2 partir de la premiere prise de nsurriture. Dans la premiere experience, nsus avons etudie la reaction la photoperiode de croisements purs et rbciproques de saumon quinnat fa chair rouge et 2 chair blanche de la riviere Quesnel (saumon de cours d'eau). Dans la deuxiPrne exp4rience, nous avons 6tudie la reaction 2 6a photoperiode de croisements purs et reciproques entre le saumon quinnat de la riviPre Quesnel (saumon de coktrs d'eau) et de la riviPre Conurna (saurnon oceanique), Dans les deux exp6riences, le jeune saumsn quinnat de Quesnel (A chair rouge ou 5 chair blanche) a connu un taux de croissance eleve et a manifest6 une grande facult6 d'adaptation 5 I'eau de mer uniquement lorsqu'il etait d'abord expos6 2 une photoperiode 2 phase diurne courte pendant 10 sern, puis 2 une photoperisde 2 phase diurne longue. En revanche, le saumon quinnat de la riviPre Csnuma s'est developpe rapidement et a acquis la facult6 d'adaptation fa I'eau de mer accrue caracteristique des srnolts, quel que ssit le regime de phstspkriode dans lequel il etait eleve. bes hybrides issus des eroisernents reciproques Conuma-Quesnel ont manifest6 le type dedeveloppement oeeanique, ce qui indique que le phenotype independant de la photop6riode est dominant et n'est pas determine par le g6nsme maternel.

Received October 3 1, 1 99 1 Accepted May 2 1 , 1992 (JB289)

C hinook salmon (Oncorh~~nehus tshhzwytscha) exhibit two major life history patterns with different lengths of fresh- water residence: & & ocean-type" juveniles migrate to sea

as underyearlings whereas 66s%ream-type" juveniles reside in fresh water for one or more yeas before developing into smolts a d migrating to the sea (Healey 1983, 199 1 ; Cxl md Healey 1984; Taylor 1990a). The pm-smolt trmsfomatim chaac- terized by numerous movhological md physiological changes including rapid growth and increased ability to adapt to sea- water is synchronized by the annual photoperiod cycle in var- ious salmonids (Hsx 1988; Clarke 1989). Recently, we found a difference in photoperiod response between stream- and ocean-type chinook salmon fry. Stream-type (Kitsudalum River) fry exposed to a short-day photoperiod for 2 mo fo1- lowed by exposure to a long-day photoperiod responded with the accelerated growth and development of increased seawater adaptability characteristic sf smslts whereas those exposed to a long-day photoperiod from the time sf first feeding remained

pmlike with slower growth and poor seawates adaptability (Clarke et al. 1989). In contrast, ocean-type (Big Qualicum River) fry grew well md adapted readily to seawater after either photoperiod treatment (Clarke et al. 1989).

The present investigation was undertaken to detemine the genetic basis for variation among chinook salmon populations with respect to photope~od control sf smelting. Two experi- ments were conducted. The first was conducted to detemine whether red- and white-fleshed chinook salmon from the Ques- nel River have different responses to long- and short-day treat- ment. Although the determination of red and white flesh colour in Quesnel River chinook salmon is under genetic control (Withler 19861, it is not known whether the two phenotypes belong to a single polymorphic population or to two sub- populations with restricted gene interchange. The second experiment tested the photoperiod responses sf crosses among Quesnel River (stream-type) and Conuma River (ocean-type) chinook salmon.

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Materiais and Methds

Experiment 1

Adult chinook salmon captured in the Quesnel River, a tributary of the upper Fraser River, were classified as "reed" (R) or "white9' (W) on the basis of external skin colour and flesh colour (Withler Z 986). Gametes were collected from each sf four white females, white males, red females, and red males. Eggs and milt were transported separately to the Wosewall Creek Hatchery on Vancouver Island and then fertilized in an 8 X 8 facto~al design to produce four cross types: X w, X R, R x W, and R x W. Thus, ezch cross type included 16 families of fish. Hn late January, fry were removed from the incubation trays and transpasfie8 t s the Pacific Biological Station. A group of $0 fry from each cross type was placed in a 197-L tank in each of two separate rooms. Fry in one room received a short- day photoperiod (9.5 h light : 14.5 h dark) and in the second a long-day one (14.5 h light : Q e . 5 h dark) which was equivalent to natural daylength plus civil twilight on April 10. These photoperiods were maintained until April 10 and then both rooms received a simulated natural photoperiod cycle increasing from 14.5 h light : 9.5 h dark. Fry were hand-fed with Ewos starter diet initially, and then White Crest feed was delivered using automatic feeders throughout the daylight hours at 1.5 times the level recommended by the manufacturers, with pellet size adjusted as fish grew. Water temperature was held at 10°C until June 23 when the water supply was switched to 29% seawater at 24'C. The fish were maintained until November 16. Weight md length measurements were made on all fish in each tank on Mach 5, April 2, April 30, May 28, and June 119 (fresh water) and July 2, July 30, and August 14 (salt water). Samples sf 18 fish per tank were removed for 24-h seawater challenge tests (Blackbum and Clarke 1987) on April 22, May 14, June 8, and June 22. The following analysis of variance (MOVA) model was used to examine variation in weight, length, growth rate, and plasma sodium levels for the fish in this experiment:

Y.. = p + Pi f c, + P C , , f elj,

where YUk is the individual measurement, p is the overall mean, Pi is the fixed effect of photoperiod (i = 1, 21, C j is the fixed effect of cross type (j = 1, 41, PC., is the interaction between photoperiod and cross type, and e , is the error tern of the kfh observation in subgroup i jk.

Experiment 2

Gametes were collected from adult chinook salmon captured in the Quesnel River (Q) and at the Conuma River (C) enhance- ment facility on the west coast of Vancouver Island. Eggs and milt were taken from nine males and nine females of each stock. Gametes from the Qasesnel River population were obtained from both red and white males and females. The gametes were trans- ported separately to the Pacific Biological Station where they were fertilized in three sets sf 6 x 6 crosses to produce four cross types: C x C, C x Q, Q x C , and Q x Q . Within each of the three sets, nine families of each cross type were created (three males by three females). This was done to ensure an adequate sample of the genetic variation within the two wild populations so that differences among cross types are more likely to reflect differences between populations rather than among individuals within populations. Family identity was not maintained past incubation, but the group of fry representing each replicate group of each cross type consisted of equal wum-

bers of fq from all 27 families (three sets by nine crosses) of that cross type. On Jmuq 18, fay were removed from the incubation trays and 150 fry from each cross type were placed in each of two replicate 197-L tanks in each of two separate rooms. Fay in one room received a short-day photoperiod (10 h light : 14 h dark) md in the second a long-day photoperiod ( 14 h light : I0 h dark). The photoperiod levels were held con- stant until April 1 when both rooms were switched to a simu- lated natural photoperid increasing from 14 h light : 10 h dark. The actual daylengths were adjusted slightly from those in experiment 1 in order that the long-day photoperiod would coincide with natural daylength plus civil twilight on April 1. Water temperature was 11°C until June 23 when the incoming water supply was switched to 29%0 seawater at 14OG.

On March 29, 28 fish in each tank were implanted intraperi- toneally with PIT tags (Destrora Identification Devices, Inc. ) in order that individual growth rates could be determined. Weight measurements on the PIT-tagged fish were taken on April 5, June 22, June 24, and November 16 and were used to calculate the instantaneous freshwater (April 5 - Sune 22) and seawater (Sune 24 - November 16) growth rates. The following ANOVA model was used to examine variability in growth rates in fresh and salt water as well as weight at the end of the experiment on November 16:

where Yuk, is the individual measurement, p is the overall mean; Pi is the fixed effect of photoperiod (i = I , 2), C, is the fixed effect of cross type (j = 1, 41, P C , is the interaction between photoperiod and cross type, Ruk is replicate of subgroup ig' ( k = 1, 21, and ew is the error term of the hh observation in subgroup ijk.

Samples of five fish from each tank were removed for 24-h seawater challenge tests in March, April, and May; a sample of 12 fish was taken from each tank for a seawater challenge test on 19 June, just prior to transfer sf the remaining fish to seawater. Fish from replicate tanks were combined for the chal- lenge tests, so variability in the plasma sodium levels was examined using the following ANOVA model:

where Ygk, is the individual sodium measurement, p is the over- all mean; Pi is the fixed effect of photoperiod ( i = 1, %), C . is the fixed effect of cross type (j = 1, 4), D, is the fixed effkct of sampling date (k = 1, 4), P C , is the interaction between photoperiod and cross type, and e,, is the error tern of the hh observation in subgroup ijk.

Experiment 1

Growth in weight was similar among d l four flesh colcsur groups under both photoperiod treatments during February, March, and April (Fig. 1). During this period, the mean specific growth rate for weight did not vary significantly with photoperiod treatment (F , , , = 2.87, p 8.01) (Table I). However, during May and Sune, fish previously exposed to the short-day photoperiod grew I -6 times as fasB(F, 7 , = 101.82, p < 8.005) as did the fish exposed to long-day photoperiod (data not shown). During the final 6 wk in seawater, the short- day fish grew 2.7 times as fast (F, . , = 60.36, p < 0.005) as the long-day fish (Table 1). As a result, the short-day fish had a significantly greater fork length (F,,, = 58.96, p < 0.005),

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601 SHORT DAY

FEB 3 MAR 5 APW 2 APW 38 MAY28 JUNIS JUL2 JULX AUG 14

FIG. I . Influence of long- and short-day photopefiod treatments for 10 wk from the time of first feeding on subsequent growth in fresh and salt water sf progeny of crosses among red- (8) and white-fleshed (W) stseamtype chinook salmon from the Quesnel River.

weight (F,,, = 31.05, p < 0.025), and condition factor (F,,, = 41.03, p < 0.81) at the end of the experiment on August 14 (Table 1). In contrast, there were no significant differences due to ersss type with respect to fork length (F,,, = 1.4, p > 0.25), weight (F,?, - 1.25, p > 0.23, or condition factor (%;3,3 = 3 -28, p > 0. I) on August 14. As with the growth responses, seawater adaptability as judged by plasma sodium levels after 24-h seawater challenge tests was significantly affected by photoperiod (F,,, = 45.23, p < 0.01) but not by cross type (F3,, = 1.13, p > 0.25) (Table 2). On the one hand, the long-day fish did not regulate plasma sodium concentrations below 170 mmol-L-' during any of the challenge tests. On the other hmd, the short-day fish regulated plasma sodium Levels belaw I70 mmol-l - "uring May and

June, indicating a high degree of seawater adaptability. This difference in seawater adaptability was not related to size variation between photoperiod treatments, since there was no significant coneHation between fork length and plasma sodium concentration in the May and June tests for either the long-day (r = 0.07, n = 118)orshokt-day fish (r = -0.05, pe = 121). Mortality after transfer s f all fish to seawater (June 23 - August 14) was less than 5% with the exception of the R x R cross which lost 7% in the short-day group and 18% in the long-day group.

Experiment 2 Growth in weight varied little among the Quesnel, @ornuma,

and hybrid groups of chinook salmon fry on either photope~od

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TABLE 3. Specific gmwth rde (6) for weight of crosses among tagged Quesnel (stream-type) and Csnuma River (ocean-type) chinook salmon from April 5 to June 22 in fresh water (W) at 11°C and from June 24 to November 16 in seawater (SW) at 14°C. Values are given as mean + SE.

- -

cross type Gw Gsw

Photoperiod (d X 8) n (%bw-d--') n (%bw-d- I )

Long b y

Mean 1.60 1.57

TABLE 4. Fork length? wet weight, and condition factor on November 16 of crosses among Canuma (ocean-type) and Quesnel River (stream-type) chinook salmon in seawater. Values are given as mean 5 SE (replicate tanks combined).

cross Fork Condition type length Weight factor

Photoperiod (d X 6) n (m @I (IOO-W~-L-~)

Short day C X C 26 18.9 & 0.4 $8.3 i- 5.2 1.2'7 r. 0.02 C x Q 3 1 21.0 5 0.3 129.9 A 6.2 1.36 2 0.02 w e 32 21.4 A 0.2 132.5 =k 4.1 1 -34 & 0.01 Q X Q 22 22.3 5 0.5 165.4 + 8.6 1.44 + 0.02 Mean 20.9 127,9 1.35

Long day C X C 28 20.6 & 0.2 114.3 + 3.5 1.29 k 8.01 C X Q 32 22.3 & 0.3 155.7 i- 4.4 1.38 .zk 0.01 Q X C 35 22.0 iz 8.3 148.8iz6.2 1 .38&0.02 Q X Q 2 24.3 c 0.1 204.0 &. 9.4 1-42 2 0.05 Mean 21.7 142.3 1.35

June (Table 5). As in experiment 1, the Q x Q cross showed poor seawater adaptability after Iong-day treatment whereas the C X C, C x Q , and Q X C groups had developed a high degree of seawater adaptability typical of smelts. As a result, ANOVA for plasma sodium data from dl four seawater chal- lenge tests indicated a significant interaction between photo- period and cross type (F,,,, = 20.8, p < 0.001). One-way ANBVAs for cross type run independently for each photo- period for combined results from the May and June tests revealed no effect of cross type on seawater adaptability in response to short-day photopiod (F;, 125 = 1 .O I , p > 8.25). In contrast, there was a significant effect of cross type sn sea- water adaptability during May and June after long-day treat- ment (F3,,,, = 28.68, g < 0.001). This effect of cross type under long-day photoperid was still highly significant (F3, ns = 27.5, p < 0.00 1) after analysis using fork Length as a covaiate, indicating that it was not due primarily to size differences.

Discussion

In both experiments, Quesnel chinook salmon fry sustained a rapid growth rate and developed a high degree of seawater adaptability only when exposed first to a short-day photopehiod and then to a lsng-day photoperiod. Clark and Shelbum (1986) hypothesized that coho salmon (Onesrhynchkss kisutch) fry

require a period of exposure to short-day photoperiod from the time of first feeding in order to develop uniformly as zero-age smelts, This requirement for exposure to a short-day photo- period for srnolting has since k e n confirmed in studies with coho and strearn-type chinook salmon fry (Clarke et al. 1989; Thoruensen and Clarke B 989; Thorarensen et al. 1989) as well as in the current study. This developmental switch in stream- type chinook salmon ~espsnds specificalically to daylength expe- rience following emergence; it determines whether they will develop as srnslts or remain as p m during the following sum- mer. Under natural conditions where emergence wcurs under a long-day photoperiod, it causes juveniles to overwinter in fresh water for at Beast 1 yr before becoming smolts. However, ocean-type chinook salmon do not share this requirement as shown by the growth and development sf the Conuma River fry under either photoperiod regime. The response of the Con- uma River fry is consistent with that obbsewed previously in experiments using ocem-type chinook salmon fmm the Big Qualicum River (Clarke et al. 1989) and with the srnolting of these ppulations as undeqealings under natural rearing eon- ditions (Healey 199 1 ; Taylor 1990~1).

Although differences in flesh colour among chinook salmon from the Quesnel River have a genetic basis (Withler 19861, the results of experiment 1 indicate that red- and white-fleshed chinook salmon from the stream-type Quesnel River popuHation Rave the same response to photoperiod. In contrast, the results

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TABLE 5. Plasma sodium coneeatration (mol-L- ' ) after a 24-h seawktter challenge of crosses mong Cesnbama (ocean-type) and Quesnel River (stream-type) chinook salmon under two photoperiods (rep- licate tanks combined). Values are given as memi + SE. n --- 10 in each test except for June (a = 24).

Cross Test date Q'P

Photoperiod (d X 9 ) March 17 April 15 May 18 June 20 Cross mean

Long day C x C C x Q Q X C Q x Q Mean

Short day c x c C x Q Q X C Q x Q Mean

of experiment 2 demonstrate that the difference in responsive- ness to photoperid between juvenile chinook salmon with stream- and wean-type life history patterns is under genetic control. Fry from both reciprocal Quesnel4cswuma hybrid groups displayed the ocean-type pattern of development. This indicates that the photopePiod-independent phenotype is dom- inant and not under maternal control. 'The dependence of growth and smolting in stream-type chinook salmon on photoperiod, md the absence sf a p h o t o p ~ d effect on developmental rate in oceam-type chinook salmon, illustrates a genotypeenviron- ment interaction. To our knowledge, this is the first time that genetic control of qualitatively different patterns of growth and smolting hasbeen shown for any salmonid. H d e et al. (1989) reported a genotype X environment interaction in presmolt Atlantic salmon (Sakmo salar) that resulted from a change in the magnitude of the growth response of individual families to a long-day photoperiod during autumn. Within photoperiod treatments, reciprocd hybrid goups were intermediate in their length a d weight compared with the pure strains, as would be expected from additive genetic inheritance of growth rate.

In a review of the geographic distribution of these two juve- nile life history types in chinook salmon, Taylor (19Wa) sug- gested that variation in age at smolting among populations is controlled in part by environmental moduhtion (Smith-Gill 1983) of smelting rate though variability in growth opportunity md that this control may be limited by selection for size at migration. Although we agree that variation within each life history type is influenced considerably by differences in growth opprtaanity, it does not cause a change from one life history type to the other. The present study has demonstrated the exist- ence of a developmental switch, present in stream-type but lacking in ocem-type chinook salmon, that responds specifi- cally to daylength experience in the months after emergence. Patterns of growth and seawater adaptability of stream-type chi- nook sdmon during the subsequent summer are determined by the developmental path taken rather than by growth opportu- nity . Therefore, we conclude that the difference in juvenile life histories between ocean-type and stream-type chinook salmon results from developmental conversion (Smith-Gill 1983) rather than phenotypic modulation.

In addition to differences in smolting patterns, earlier inves- tigations have reported variation in morphology (Carl and Healey 2984) as well as rheotactic and agowistic bekaviours (Taylor and Lakin 1986) between stream-type and ocean-type

chinook salmon fry. However, the shift from juvenile to adult haemoglobin patterns did not vary between the two life history types, nor was it correlated with smoltification (Fyhn et al. 1991). In an earlier study sf six populations of chinook salm~n, we did not observe a significant difference in weight between fry from ocean- and stream-type populations given early expo- sure to a Iong-day photoperiod, nor significant additive genetic variation for weight within populations, after 100 d of rearing in fresh water (Withler et al. 1987). In retrospect, it would seem that the 7-8°C water temperatures used in that experiment were too low to allow expression of the greater growth potential of ocem-type chinook salmon fry when reared under ambient pho- toperiod. In contrast, Cheng et al. (1987) observed a strong additive genetic effect on growth both in fresh md in salt water of progeny fmm crosses between two populations of ocean-type chinook salmon. In a study of four populations from each life history type reared in the laboratory under simulated natural photoperiod, Taylor (1 990b) found that ocean-type chinook salmon grew more rapidly than did strem-type. Riddell md Sorensen (1986) reported that hybrid yearling coho salmon had growth rates in fresh water that were intemediate to those of the purebred parental strains.

Similarly, quantitative genetic variation for smolting has been observed in accelerated zero-age coho sdmon (Saxton et al. 1984; R. E. Withler, unpubl. data). Wefstie et al. (1977) reported considerable genetic variation in the proportion of 1-yr smolts among 37 stocks sf Atlantic salmon; this proportion was highly correlated with average weight, possibly because they defined a smolt as a fish retained by a IO-rnm grader in Mach. Thorpe and Morgan (1978) demonstrated genetic var- iation in the proportion sf potential yearling smolts among four half-sib families of Atlantic salmon.

The complete dominance of the photopiod-independent phenotype in hybrid chinook salmon juveniles indicates that photspefiod responsiveness may be under Mendelian genetic control. Nevertheless, we cannot exclude the possibility that it is a threshold trait under quantitative control. Segregation of the photopendod-dependent a d -independent phenotypes among F2 md backcross progeny is being examined in order to solve this question. Although not previously demonstrated in salmon, genetic c o n t ~ ~ l of responsiveness to short-day photoperiods has been reported in the Djungaim hamster (Phdogrus sungorus S U F Z ~ Q T U S ) by hchdsky and Lynch (1 986, B 988); responsive and nomsponsive hamsters also differed in their expression sf

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circadian rhythmicity when held under a short-day photoperid. Studies of mutants that affect circadian clock properties in var- ious organisms over the past 50 yr have revealed different modes of genetic control ranging from single to multiple genes (Feldrnan 1983). When short-period mutants of Chlamydo- monas were crossed with the wild-type form, a 5050 dist-i- bution sf phenotypes was obtained, demonstrating Mendelian inheritance (Mergenhagen 1984). If photoperiod resgonsive- ness in chinook salmon is in fact controlled by a single gene, it is conceivable that stream-type races may have arisen repeat- edly by disruptive selection in scean-type populations (see Healey 199 1) .

W e are indebted ta G. Johnston and A. Solmie for assistance with b r o d s t w k co11ection and egg incubation and to J. Blackbum, B. B m o n , G . Jestin, md L. Naylsr for technical help throughout the study. This paper benefitted from critical reviews by Drs. C. J . F m t e md E. B. Taylor.

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