evidence for inheritance of age of maturity in chinook salmon ( oncorhynchus...

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Article The Rockefeller University Press $30.00 J. Exp. Med. 2014 www.jem.org/cgi/doi/10.1084/jem.20140455 Cite by DOI: 10.1084/jem.20140455 of 7 Inflammation is a normal physiological response to tissue injury caused by infections, burns, trauma, and other insults.Tight regulation of this response is important for initial recognition of danger signals, elimination of the causative lesion, and restoration of tissue homeostasis (Serhan et al., 2010).This involves a complex cascade of events including recruitment of neutrophils, basophils, monocytes, macrophages, and CD4 + and CD8 + T lymphocytes to the site of injury.These infil- trates release soluble mediators (histamine, leu- kotrienes, and nitric oxide), cytokines (TNF, IFN-, and IL-1), chemokines (IL-8, MCP1, and KC), and enzymes (lysosomal proteases) that together establish and amplify the inflammatory response.Timely production of antiinflammatory molecules (PGE2, IL-10, TGF-, and IL-1R) dampens and terminates this response (Lawrence et al., 2002). In the presence of persistent tissue injury or of an unusual infectious/environmental insult, overexpression of proinflammatory me- diators or insufficient production of antiinflam- matory signals results in an acute or chronic state of inflammation (Serhan et al., 2010). Acute inflammatory conditions, such as septic shock and encephalitis, are difficult to manage clini- cally and have high mortality rates. Chronic in- flammatory diseases such as rheumatoid arthritis (RA; Majithia and Geraci, 2007), inflammatory bowel disease (IBD; Loftus, 2004), systemic lupus erythematosus (SLE; Rahman and Isenberg, 2008), psoriasis (PS; Gelfand et al., 2005), mul- tiple sclerosis (MS; Ramagopalan et al., 2010), type 1 diabetes (T1D; Green et al., 2000), and CORRESPONDENCE Philippe Gros: [email protected] Abbreviations used: CCD, coiled-coil domain; CCDC88B, CCD containing protein 88B; ChIP, chromatin immuno- precipitation; CM, cerebral malaria; ECM, experimental CM; ENU, N-ethyl-N-nitrosourea; GWAS, genome-wide associa- tion studies; HA, hemagglutinin; IBD, inflammatory bowel dis- ease Iono, Ionomycin; IRF1/8, interferon regulatory factor-1/8; KC, keratinocyte chemoattrac- tant; LD, linkage disequilibrium; LOD, logarithm of odds; LT, lymphotoxin ; MBD, micro- tubule binding domain; MCP-1, monocyte chemoattractant protein-1; MS, multiple sclero- sis; P.bA, Plasmodium berghei ANKA; PBC, primary biliary cirrhosis; PGE2, prostaglandin E2; PMA, phorbol 12-myristate 13-acetate; PS, psoriasis; PTS, peroxisomal targeting sequence; RA, rheumatoid arthritis; SC, sarcoidosis; SLE, systemic lupus erythematosus; STAT1, signal transducer and activator of tran- scription 1; T1D, type 1 diabetes. *J.M. Kennedy and N. Fodil contributed equally to this paper. CCDC88B is a novel regulator of maturation and effector functions of T cells during pathological inflammation James M. Kennedy, 1,4 * Nassima Fodil, 1,4 * Sabrina Torre, 2,4 Silayuv E. Bongfen, 1,4 Jean-Frédéric Olivier, 1,4 Vicki Leung, 2,4 David Langlais, 1,4 Charles Meunier, 1,4 Joanne Berghout, 1,4 Pinky Langat, 1,4 Jeremy Schwartzentruber, 3 Jacek Majewski, 2,3 Mark Lathrop, 2,3 Silvia M. Vidal, 1,2,4 and Philippe Gros 1,2,4 1 Department of Biochemistry, 2 Department of Human Genetics, 3 McGill and Genome Quebec Innovation Center, 4 Complex Traits Group, McGill University, Montreal, Quebec H3A 0G4, Canada We used a genome-wide screen in mutagenized mice to identify genes which inactivation protects against lethal neuroinflammation during experimental cerebral malaria (ECM). We identified an ECM-protective mutation in coiled-coil domain containing protein 88b (Ccdc88b), a poorly annotated gene that is found expressed specifically in spleen, bone marrow, lymph nodes, and thymus. The CCDC88B protein is abundantly expressed in immune cells, including both CD4 + and CD8 + T lymphocytes, and in myeloid cells, and loss of CCDC88B protein expression has pleiotropic effects on T lymphocyte functions, including impaired maturation in vivo, significantly reduced activation, reduced cell division as well as impaired cytokine production (IFN- and TNF) in response to T cell receptor engage- ment, or to nonspecific stimuli in vitro, and during the course of P. berghei infection in vivo. This identifies CCDC88B as a novel and important regulator of T cell function. The human CCDC88B gene maps to the q3 locus that is associated with susceptibility to several inflammatory and auto-immune disorders. Our findings strongly suggest that CCDC88B is the morbid gene underlying the pleiotropic effect of the q3 locus on inflammation. © 2014 Kennedy et al. This article is distributed under the terms of an Attribution– Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial– Share Alike 3.0 Unported license, as described at http://creativecommons.org/ licenses/by-nc-sa/3.0/). The Journal of Experimental Medicine on November 23, 2014 jem.rupress.org Downloaded from Published November 17, 2014

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Page 1: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

Evidence for Inheritance of Age of Maturity in Chinook Sa Oncorhynchus tsha wytscha

David G . Mankin Department of Fisheries, Hurnboldt State University, Arsata, CA 9552 1 , USA

jay W. Nicholas Oregon Department sf Fish and Wld%ife, 850 Ska' 15th Street, Corvallis, OR 97333, USA

and Timothy W. Downey

Oregon Department of Fish and Wildlife, 3 150 East Main Street, Springfield, 0 8 97478, USA

Hankin, D. G., 1. W. Nicholas, and T. W. Downey. 1993. Evidence for inheritance of age of maturity in chinook salmon (Oncorhynchus tshawytscha). Can. 1. Fish. Aquat. Sci. 58: 347-358.

We report results of age-specific mating experiments carried out with chinook salmon (Oncorhynchus tshawy- tscha) at Elk River Hatchery, Oregon. Our analysis of returns from these experiments includes assessment of the marine growth of progeny, and we also account for the negative bias on mean age of returning mature progeny that is a consequence of troll fishery harvest of immature salmon. Results suggest that (aj heritability of age of maturity is relatively high in this species (calculated h' were 0.49-0.57 and 0.39-8.44 for males and females, respectively), (b) inheritance of age sf maturity of females appears to be independent of age of male parent, and (c) for a given parental age, "faster-growing" progeny generally mature at younger ages, but (d) progeny from older parents are not generally smaller at age than progeny from younger parents. Inheritance of age of maturity therefore cannot be a simple reflection of inheritance of growth rate. We tentatively propose the existence of heritable minimum threshold lengths that differentially trigger maturation according to age and sex of parents. We also consider the significance of these experiments for artificial propagation of this species.

Nous presentons les resultats d'essais de reproduction specifiques quant 2 l'dge chez le saumon quinnat (8ncca- rhynchus tshawytscha) qui ont 6t6 realis& a la pisciculture de Elk River (Oregon). Notre analyse des remontees suite 2 ces essais comporte l'6valuation de la croissance en mer de la progeniture et tient compte du biais negatif sur I'ige moyen de la progkniture mature des remontees qui decouie de la capture de saumons immature5 par la pGche A la cuiller. Les resultats obtenus portent a crsireque a) l'heritabilitede I'age a la maturite est relativement elevee chez cette espgce (hh calcules des males et des fernelles de, respectivement, 0,49-0,57 et 0,39-63,44), b) I'hkritabilite de ['Age 2 %a maturite des femelles semble etre independante de ['Age du parent m2Je et c) pour un Age parental donne, la progeniture a croissance "plus rapide" mature generalement a un dge plus jeune, mais que d) la progkniture des parents plus 2ges n'est pas, de faeon generale, plus petite aux mGmes 2ges que celle de parents plus jeunes. L'hkritabilitk de l'age de la maturite n'est donc pas une simple fonction de l'heritabilite du taux de crsissance. Nous forrnulons lPhypoth$se qu'il existe des longueurs seuils hkreditaires qui provoquent, de faeon differentielle, la maturation en fonction de l'age et du sexe des parents. Nous examinons aussi I' incidence de ces resultats dans le contexte de la propagation artificielle de cette esp&ce.

Received March 7 4, 1 99 9 Accepted September 29, 7 992 (JA94.3)

0 f the semelpxous species of the genus BncorBzynchus, the chinook salmon (8 . tshawytscha) displays the largest variation in duration of marine residence and

size at maturity (Healey 1991). Male chinook salmon may mature as early as age 2 (as "jacks") at a size of about 2 kg, through at least age 7 at sizes up to 50 kg. Although female chinook salmon only rarely mature at age 2, they may mature from age 3 through at least age 7 at sizes ranging from about 3 to 50 kg. Across their geographic range, chinook salmon stocks exhibit wide variation in mean age of maturity (Healey 1991) and in the relative tendency to produce jacks. For exam- ple, Nicholas and Hankin (1988) classified Oregon coastal chi- nook salmon stocks into early-, mid-, and late-maturing stock types, largely on the basis of mean age of female maturation. In early-maturing Oregon stock types, substantial proportions of females mature at age 3 whereas in mid- and late-maturing

Resu ie 74 mars 7 99 7 Accept6 ie 2 9 septembre 1 99 1

stock types, few females mature at age 3 and the majority of females mature at ages 4 and 5, respectively. Tendency of stocks to produce age 2 male jacks is not, however, strongly correlated with mean age of female maturation. Some early- maturing stocks produce relatively few jacks (e. g . Klamath RiverJIron Gate Hatchery, California, fall chinook salmon; Hankin 1990) whereas some late-maturing stocks produce large numbers of jacks (e.g. Salmon River, Oregon, fall chinook salmon; Nicholas and Hankin 1988).

Although age of maturity is a complex character that varies in a discontinuous (i.e. integer) manner and is presumably influenced by many genes, inheritance of such a "threshold" character can be approached using the basic methods of quan- titative genetics (Falconer 198 1, chap. 18). In particular, two contrasting groups of parents of known (but different) ages of maturity (phenotype) may be mated with one another. The

Can. 9. Fish. Aquar. Sci., Vok. 50, 199.3 347

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Page 2: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

TABLE 1. Number, date, mark, and average size at release (g) for offspring from three age-specific mating experiments conducted with fall chinook salmon at Elk River Hatchery, Oregon. RV and LV denote right and left ventral fin clips, respectively; 4 + denotes ages 4-4 (see Table 2 for age distributions).

Age of parents

Brood Date Number year Male Female Mark released Size released

1974 3 3 LV 20 Oct. 1975 42.8 171335 5 5 WV 20 Oct. 1975 40.9 31401

1979 2 4 + RV 14 Oct. 1980 35.5 7 1943 4-1- 4 + LV 14 Oct. 1980 34.9 53'742

1980 2 4 + RV 27 Sept. 198 1 30.7 105084 4 + 4 + LV 27 Sept. 198 1 31.7 114528

TABLE 2. Number of parents by age and sex used in three age-specific mating experiments conducted with 1974, 1979, and 1980 brood year fall chinook salmon at Elk River Hatchery, Oregon. 3 X 3 denotes age 3 male (M) and female (F) parents; 5 X 5 denotes age 5 male and female parents; 2 x 4 + denotes age 2 male and age 4-4 female parents; 4 + X 4 + denotes age 4-6 male and age 4-4 female parents.

1974 brood year 1979 brmd year 1980 brood year

3 x 3 5 x 5 2 x 4 + 4 + x 4-4- 2 x 4 + 4 + x 4 + Age of parents M H M F M F M F M F M F

Total 55 55 9 9 26 17 3 5 16 27 2'7 27 2'7 Mean age 3.0 3.0 5.0 5.0 2.0 4-18 4.23 4.06 2.0 4.81 4.58 4.89

between-group difference in mean age of maturity among the progeny that results from these matings is interpreted as the response to selection (difference beween mean parental ages) and allows calculation of heritability ((Falconer 198 1, chap. 1 1).

Ricker (1972) summarized the then available information on inheritance of age of maturity in chinook salmon based on such "age-specific mating experiments" (see Ellis and Noble 1960, 2961 ; Bonaldssn and Menasveta 196 1 ; Bonaldson and Bonham 1970). He concluded that the genetic influence on age of matu- rity is strong and that male and female ages are to some extent determined independently. Generally, older (and lager) par- ents produced progeny that matured at older ages and larger sizes than did younger (and smaller) parents.

Inheritance of age of maturity of chinook salmon has sub- stantial importance for fishery management because size-selec- tive commercial and sport fisheries shift the age composition of spawning runs toward younger and smaller fish. Rutter (1904) noted that the selective removal of older and larger fish in freshwater gillnet fisheries resulted in an unnatural abun- dance of jacks among escaping spawners. He was apparently the first fishery scientist to express concern that this shift in age structure of spawners might lead to a greater tendency of stocks to produce less valuable jacks. In ocean troll fisheries, imma- ture chinook salmon become vulnerable to capture when they first exceed minimum size limits. Such legal-sized but imma- ture fish are often caught at an age that is several years younger than their predestined age at maturity. Cleaver ( 1969), Ricker (1980), and Hankin and Healey (1986) described how these ocean tro11 fisheries, through their cumulative removals of immature fish, shift age composition of spawning runs toward

younger (and smaller) fish and shift sex composition toward males.

Ricker (1980, 1981) expressed concerns that these troll- fishery-induced shifts toward younger spawners could produce genetic shifts toward younger age of maturity in chinook salmon stocks. He speculated that reduced mean age of maturity might reduce stock productivity and that smaller females might not take full advantage of large spawning gravels in large turbulent streams. Hankin and McKelvey (1 985) elaborated on this theme and noted that larger females generally have larger eggs than smaller females (see also Beacham and Murray 19983); larger females probably dig deeper nests than snaaller females, thus making their eggs less susceptible to damage due to bed load movement during storm events; larger males are behaviorally dominant and enjoy much greater spawning success than smaller males (see Baxter 199 I) , presumably indicative of their relative "fitness"; and the energetic requirements of long-~Hs- tance migrations may favor larger adults. In response, Healey and Heard (1985) expressed concern regarding the economic consequences of reduced size and age of chinook in fisheries, but they constructed alternative arguments suggesting that smaller chinook may be no less "fit" than larger chinook. In support of their contention, they observed that the age com- position of any spawning mn must be a "compromise among the conflicting advantages to large and small size." Improved understanding of the inheritance of age of maturity in this spe- cies should help determine which of these alternative positions is more tenable.

In this paper, we present results from age-specific mating experiments conducted with 1974, 1979, and 1988 brood year

Can. J . Fish. Aquat. Sci., V01. 50, 6993

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Page 3: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

TABLE 3. Coded wire tag (CWT) recovery data for 1974 brood year releases of CWT-marked fall chinook salmon released from Elk River Hatchery, Oregon, in October 1975 (pooled estimated recov- eries at age ~f fish belonging to CWT groups 07- 10-09 and 07-10-15; 61 366 fish released from both groups combined in October of 1975) and resulting estimates of age-specific ocean fishery exploitation rates. Estimated expl~itation rates are based on assumed annual conditional ocean survival rates (sur- vival rates from end of fishing season in year i until beginning of fishing season in year i + I) of 0.5 from age 2 to 3 and 0.8 for older ages. Methods used to calculate ocean fishery exploitation rates are from Hankin (1990, appendix).

Year of return Ocean catch Freshwater Exploitation or capture Age at age escapement rate

TABLE 4. Sample sources and sample sizes for scale measurements displayed in Fig. 2, and mean MEPS lengths (mm) at maturity by age and sex (M = male, F = female) for 1974 brood year matings of age 3 males with age 3 females (3 X 3) and age 5 males with age 5 females (5 X 5) . Standard deviations in ~arentheses.

Sample source

Spawning Estuary Age Mating Sex Hatchery survey tagging Total Mean length

fall chinook salmon reared and released at Elk River Hatchery, Oregon. Our mating experiments and our analyses of data from these experiments differ from those previously reported (see Ricker 1972, table XI) in several important respects. First, dif- ferences between mean parent ages of mating groups in our experiments were generally 2 yr whereas differences were gen- erally less than 2 yr in earlier experiments. Second, we released groups of fish with contrasting known-age parents from the same brood years whereas in some earlier experiments, fish were sometimes released from different brood years. When progeny from different-aged parents are released in different brood years, the effects of parent age and brood year are con- founded: between-group differences in progeny phenotypes may reflect differences in environmental conditions experi- enced by groups as much as or more than between-group dif- ferences in parental age. Third, our analyses of returns from experimental releases included assessment of the marine growth of fish that matured at different ages. Finally, we also account for the negative bias (Wicker 1980) on mean age of returning mature fish that is a consequence of cumulative troll fishery removals of immature fish. To our knowledge, these last two factors have nut been examined in previously published analyses.

Methods

Matings, Wearing, and Release

We designate age by the difference between parental brood year and progeny year of life or year at maturity. Thus, for example, a 1988 brood year fish alive in the ocean or returning to freshwater in 1992 is designated age 4.

Age-specific mating experiments were conducted with 1974, 1979, and 1980 brood year fall chinook salmon (Elk River stock) at Elk Wiver Hatchery, Oregon. Elk River Hatchery first began operation with collection and spawning of wild Elk River fall chinook salmon in fa11 of 1968. Elk River chinook salmon are a midmaturing, north-migrating stock type in the jargon of Nicholas and Hankin (1988). Females mature at ages 3-7, with ages 4 and 5 generally dominating brood year returns of females; males mature at aags 2-7, and jack maturation is usually substantial. Jacks accounted for more than 50% of brood year male returns from the 1968-77 brood years (Nicholas and Hankin 1988, p. $3). Ocean catches sf Elk River chinook are made in Oregon, Washington, British Columbia, and Alaska; Oregon catches consist principally of maturing fish returning to Elk River.

Can. 9. Fish. Aquat. Sci., Vol. 50, 1993

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Page 4: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

TABLE 5. Mark-recapture data and resulting estimates of river returns by age of progeny resulting from age-specific matings of fall chinook salmon at Elk River Hatchery, Oregon. 3 x 3 denotes matings of age 3 males with age 3 females; 5 x 5 denotes matings of age 5 males with age 5 females. When number of tag recoveries was less than seven, an alternative method for estimation of river returns was used (see text for explanation); this method did not allow for determination of errors of estimation.

95 % confidence limits

Return Number Number Tags Estimated year Age tagged sampled recovired return Lower Upper

In 1974, age 3 males were mated with age 3 females in one experimental group (3 x 3), and age 5 males were mated with age 5 females in a second experimental group (5 X 5 ) . In 1979 and 1980, age 2 males (jacks) were mated with age 4 and older females in one experimental group (2 x 4 + ), and age 4 and older males were mated with age 4 and older females in a second experimental group ( 4 + x 4 + ) (Table 1). Males and females were aged at time of spawning by length and/or by unique fin clips which identified brood year. Ages were later verified (1974 brood year) andlor determined (1979 and 1980 brood year) by scale reading. Numbers and ages of male and female parents for each experimental group are listed in Table 2.

Males and females were mated In pairs for the 19'74 and 1988 brood year experiments, but in 1979, sperm from 3- 10 males were pooled prior to fertilization of eggs from a similar number of females during spawning activities. If sperm from all males in each such mating group were equally viable, then each male in a group theoretically fertilized eggs from each female in that same group. (Recent reports suggest. however, that male contributions were probably not equal when sperm were pooled (see Gharrett and Shirley 1985; Withler l988).) Eggs from individual females were separately incubated in all brood years, allowing progeny from specific matings to be selected after ages of fish were verified. For the 1974 and 1980 brood years, all fry from all females within an experimental group were placed in rectangular Burrows ponds (one for each group) for rearing. For the 1979 broad year, however, available pond capacity restricted fry numbers to those from about 15 females. Thus, for the 1979 brood year experiments, more male than female parents are represented in mating experiments (Table 2). Surviving fingerlings were fin-marked (right or left ventral fin clips, RV s r EV) during midsummer and were released as subyealing smslts during early fall. Estimated numbers released from each group were calculated as the difference between the numbers marked and the numbers of daily mortalities recorded fmm the time of making until release.

Recovery Data

Mark-recapture estimates of freshwater returns were made during 1976-80 for returns of age 2-6 mature fish from the 1974 brood experimental groups. For these estimates, approx- imately 10% of the total run of fall chinook salmon was tagged in the Elk River estuary annually (1976-SO), with seining and tagging distributed throughout the spawning run (October through mid-January). Fish were tagged with numbered Beter- son discs and released for upstream migration. Recovery sam- ples consisted sf all fish that returned to Elk River Hatchery and carcasses found on the spawning grounds during weekly spawning surveys. Sex, identifying fin clips, and fork or MEPS length (mideye to posterior scale, Rei~ners 1970) were recorded for all fish tagged or examined for tags, and scale samples for age determination were removed from the key scale area from all fish examined.

Through the 1980 brood year, all chinook salmon released from Elk River Hatchery received some identifying fin clip- At several levels of resolution (i.e. total returns of hatchery fish, total returns of age i hatchery fish, returns of age i hatchery fish belonging to an experimental group), freshwater returns were generally estimated using (Ricker 1975)

where N = freshwater returns, M = number tagged, C = number sampled for tags, and R = number of tags recovered in C. Confidence limits for estimated freshwater returns were calculated by substitution of Poisson approximation 95% con- fidence limits for R (Ricker 1975, appendix II) in the above formula. Estimates of returns of males and females at age were calculated by multiplying the estimated total experimental group returns at age by the corresponding praportions of males or females among all fish examined during tagging and hatchery sampling that possessed the appropriate fin clip (LV or RV).

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Page 5: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

3x3 Matings I

2 250 7 5x5 Matings /

w

2 3 4 5 6 AGE AT MATURITY

FIG. 1 . Estimated age- and sex-specific returns of fa11 chinook salmon to Elk River from I974 brood year matings of age 3 males with age 3 females ( 3 x 3 matings) and age 5 males with age 5 females (5 X 5 matings). Release group sizes were 171 337 and 3 1 681 fish for the 3 x 3 and 5 x 5 groups, respectively. Estimated returns of males (open bars) at ages 2-6 were 3 194,2057,357,46, and 0, respectively, for 3 x 3 matings and 66, B 94,1$$,64, and 3, respectively, for 5 X 5 matings. Estimated'returns of females (solid bars) at ages 2-6 were 0, 1203, 1123, 106, and 10, respectively, for 3 X 3 matings and 0 , 37, 186, B 22, and 20, respectively, for 5 x 5 matings.

For returns at ages 2, 5, and 6 for the 5 x 5 group and at age 6 for the 3 x 3 group (1974 brood year), recaptures of tagged fish were too few (less than six) to allow essentially unbiased mark-recapture estimates of total freshwater returns (see Seber 2982, p. 60). Estimated returns of age 2 and 5 fish from the 5 x 5 group were calculated by multiplying (a) mark- recapture estimates of total freshwater returns sf age i hatchery fish by (b) the proportions of age i RV or LV (as appropriate) fin-clipped fish among all age i hatchery fish sampled (M + C - R ) . For age 6 returns, mark-recapture estimates of tohl returns of age 5 hatchery fish were first multiplied by the ratio of age 6 hatchery fish to age 5 hatchery fish among all age 5 and 6 hatchery fish examined to give an estimate of the total returns of age 6 hatchery fish. These estimates were then mul- tiplied by the appropriate proportions of age 6 fish possessing RV or kV fin clips among all age 6 hatchery fish examined to give estimates of age 6 returns for each experimental group.

Mark-recapture estimates of freshwater returns from the 1979 and 1980 brood yeam were not possible because the estu- ary tagging program was eliminated. For these experimental groups, only nominal freshwater recoveries (hatchery returns

plus spawning survey recoveries) could be tabulated. Scale ages and fin clips were used to separate brood years and exprimen- tal groups.

Adjustments of Recovery Data

For evaluation of " 6producton" releases, about 6 1 088 age O + chinook salmon smolts were released from Elk River Hatchery with identifying adipose fin clips and magnetic binary- coded wire tags (CWT) during October 1975 (1974 brood year). Estimates of ocean catch and freshwater escapement at age allowed estimation of annual age-specific ocean fishery explsi- tation rates for this C W release group (Table 3). We assumed that these same exploitation rates applied to progeny from 1974 brood year experimental matings that were released at approx- imately the same size and date.

We used these estimated exploitation rates to adjust recovery data from 1974 brood year experimental matings for the neg- ative bias on mean ages of freshwater returns that results from ocean fishery capture of immature chinook salmon. Two sets of adjusted recovery data were produced for returns from the 1974 brood year experimental mating groups. The first of these produced hypothetical estimates of freshwater returns at age that would have been observed had there been no ocean fishery capture of immature fish. The second produced hypothetical estimates of the number of fish destined to mature at ages 2-6 if there had been no natural mortality and no ocean fishery capture of immature fish after the cohort reached age 2.

Both sets of adjusted data first required calculation of an estimated number of fish (unsexed, or for males and females separately) from an experimental group that survived to age 2, just prior to ocean fisheries. For these calculations, we used Hankin and Healey's (1 986, p. 1747-1 749) definitions of the important parameters in a cohort representation of the life his- tory and fisheries for an exploited experimental group of chi- nook salmon: Ai = number of fish alive at age n", just prior to ocean fisheries, pi = (conditional) ocean survival rate from age i to age i + I for fish that are not caught and do not mature at age i, ui = annual ocean fishery exploitation rate for age i fish, ui = probability that an age i fish will mature at age i given that it is alive at age i and is not caught in ocean fisheries at age i (age-specific maturation probabilities), and S, = (esti- mated) freshwater returns at age i .

We assumed that all fish matured by age 6, and we set esti- mated freshwater returns at age 6 equal to A, (thus ignoring ocean fishery catches of age 6 fish). Given these definitions and assumptions, and the estimated annual ocean fishery exploitation rates presented in Table 3, the total number of fish estimated alive at age 2, A,, was calculated by successive solu- tion of the following equation (beginning at i = 5 and pro- ceeding through i = 2):

Equation ( 1 ) merely states that the total number of fish alive at age i, A i , must equal those that did not mature at age i and were not caught at age i ( A , , , / p i ) plus those that were caught at age i (ui A,) plus those that matured and entered freshwater age i (Si). Similar solutions and definitions apply for males and

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Page 6: Evidence for Inheritance of Age of Maturity in Chinook Salmon (               Oncorhynchus tshawytscha               )

TABLE 6. Hypothetical freshwater r e tms by age and sex from 1974 brood year matings of age 3 males with age 3 females (3 x 3) and age 5 males with age 5 females (5 x 5) if there were no fishery exploitation after age 2 (includes natural mortality). Based on age-specific ocean fishery exploitation rates estimated from 1974 brood year coded wire tagged recoveries of Elk River fall chinook salmon (see Table 3). Assumes annual conditional ocean survival rates sf 0.50 for age 2 fish and 0.8 for older fish. Note that sum of male and female entries at age (based on age- and sex-specific maturation probabilities) will not necessarily equal entry for total (based on age-specific maturation probabilities). Release group sizes were 171 337 and 31 601 for 3 x 3 and 5 x 5 groups, respectively. See text for explanation of calculations.

3 x 3 5 x 5 Age at maturity Male Female Total Male Female Total

Total 6705 4174 10873 Mean age at

maturity 2.67 3.72 3.07

TABLE 7. Hypothetical reconstruction of number of fish destined to mature by sex and age from 1974 brood year matings of age 3 males with age 3 females (3 x 3) and age 5 males with age 5 females 45 x 5) qthese were YMP natural mortality oaBsBlep-4) exploitation after age 2 . Based on age-specific ocean fishery exploitation rates estimated from 1974 brood year coded wire tagged recoveries of Elk River fall chinook salmon (see Table 3). Assumes annual conditional ocean survival rates of 0.50 for age 2 fish and 0.8 for older fish. Note that sum of male and female entries at age (based on age- and sex-specific maturation probabilities) does not necessarily equal entry for total (based on age-specific maturation probabilities). Release group sizes were 171 337 and 31 601 for 3 x 3 and 5 X 5 groups, respectively. See text for explanation of calculations.

3 x 3 5 x 5 Age at maturity Male Female Total Male Female Total

Total 10732 980 1 20609 204 % 2395 4434 Mean age at

maturity 2.96 3.81 3.37 4.01 4.62 4.35

TABLE 8. Calculated heritabilities for age of maturity of chinook salmon based on recovery data from the 1974 broad year mating exper- iments. Column labeled 6Adjustrnents" indicates that raw freshwater escapement estimates (none) were adjusted for ocean fishery catches (ocean catches) or for ocean fishery catches and natural mortality (ocean catches and natural mortality) prior to calculation of heritabilities.

Adjustments Males Females Combined sexes

None 0.485 0.390 0.510 Ocean catches 0.565 0.395 0.540 Ocean catches and

natural mortality 0.525 0.405 0.490

females separately (i.e. define A ,, and A ,, for numbers of females and males at age, S,, and S,, for numbers of females and males that return to freshwater at age, and CF,, and u,, for age-specific maturation probabilities of males and females, respectively). We assumed that p, = 0.50, g, = p, = p, = 0.80, and we assumed that the p, and u applied equally to both sexes,

Given estimates of the number of fish that survived to age t , age-specific maturation probabilities (or analogous sex-specific quantities) were calculated as (carets are omitted):

Once the A and ai were calculated, then a related cohort rep- resentation was used to calculate (a) the number of fish that would have matured and returned to freshwater at age i if there had been no ocean fishery capture or (b) the total number of fish, alive at age 2, that would have been "destined" to mature at age i if there had been no fishing or natural mortality from age 2 on. For example, the adjusted number of fish that would have returned to freshwater at age 4, if there had been no ocean fishing, would be

If there were also no natural mortality beyond age 2, then this same expression, but with p2 = p:, = 1, would provide the adjusted numbers destined to mature at age 4. (Refer to %Hankin and Healey 1986 for further details of the cohort representation.)

For the 1974 brood year experiment, heritabilities for age of maturity were calculated as the ratio of response (difference in mean age of maturity between progeny groups) to selection dif- ferential (difference in mean age of maturity between parental groups) following Falconer (1 98 1 , p. 172, 272). Although the selection differential was fixed at 2 yr for the 1974 brood year experiment, the above calculations produced several alternative data sets that could be used to calculate the response to selec- tion: (a) unadjusted estimated freshwater retums at age, (b) hypothetical freshwater returns adjusted for ocean fishery catches, and (c) hypothetical freshwater returns adjusted for ocean fishery catches and natural mortality.

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P - 3 4 5 3 4 5 z Annulus 3

340 1 u Females 1 I T Males T

4 5 4 5 AGE AT MATURITY

FIG. 2. Mean scale measurements in ocular units (mm after $8 X magnification) from center of focus to outer edge of annulus 2 and annulus 3, respectively, by sex and age of maturity for progeny that matured at ages 3-5 md 4-5, respectively, from 1974 brood y e a matings of age 3 males with age 3 females (open bus) and age 5 males with age 5 females (solid bas). Error bars indicate ? I standard emsr sf calculated means. Sample sizes are reported in Table 4.

Scale Measurements and Calculations of an Index sf Mean Cohort Length at Annulus 2

Table 4 lists sources of and sample sizes by age and sex for scale measurements from mature progeny from the two 1974 brood year experimental groups. Scale measurements were made in ocular units ( k 0.1 mm at 88 x magnification) from the center of the scale focus to the outer edges of annuli identified from acetate impressions of scales read on a microf- iche projector. Regenerated scales were not measured. Because mature chinook salmon exhibit substantial scale resorption prior to spawning (Chilton and Bilton 1986), thus distorting any body-scale relation, no attempt was made to back-calculate fish lengths from scale measurements. Instead, means and standard deviations of annular distances (center sf focus to outer annulus edge) were treated as indices of marine size at age. Simple P- tests were used to compare distances to annulus i for male and female fish that matured at ages greater than t within and between experimental groups.

Based on calculated numbers of fish that were destined to mature at ages 3-5, and on mean scale distances to annulus 2 for fish that matured at ages 3-5, we calculated mean cohort scale distances to the second annulus (2 complete yr of growth) for males and females, respectively, from the two experimental groups using

5

(2) 8, = 2 S: bZi i = 3 g3

where ST denotes-number (of males or females) destined to mature age a ' , and &, denotes mean scale distance to annulus 2

for fish (males or females) that matured at age f ( i = 3, 4, and 5) .

Calculations based on equation (2) excluded scale measure- ments for fish that matured at ages 2 and 6. Males that matured as jacks in early fall 1976 had not completed their second year of growth and thus had no comparable scale measurements; ns females matured at age 2 from either experimental group. Sam- ple sizes for mature age 6 fish were judged too small to generate reliable estimates of mean scale distances.

Results

1974 Brmd Year Experiment

With the exception of returns of jacks in 1976, numbers of fish examined for tags were no less than 24% of estimated total freshwater returns at age for the 3 x 3 and 5 x 5 groups (Table 5). Mean ages at maturity for estimated freshwater returns of males and females were 2.51 and 3.56 yr, respectively, for the 3 x 3 group and 3.48 and 4.34 yr, respectively, for the 5 x 5 group (Fig. 1). Mean ages for males and females combined were 2.83 and 3.85 yr for the 3 x 3 and 5 x 5 groups, respectively.

Adjustments of estimated freshwater returns at age for the negative bias produced by ocean fishery removals (Table 6) or ocean fishery removals and marine natural mortality (Table 7) resulted in increases of 0.2-0.5 yr in hypothetical mean ages at maturity of male and female progeny. Adjusted Glifferen~es between groups in mean ages at maturity for males and females were similar to unad~usted differences, however. Without any adjustments, differences between progeny groups in mean ages

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1979 BROOD 200 r------ --

I --: 2 x 4 + M a t i n g ~ I

2 3 4 5 6 AGE AT MATURITY

FIG. 3. Observed age-and sex-specific returns of fall chinook salmon to Elk River f i ~ m 1979 brood year rnatings of age 2 males with age 4-6 females (2 x 4 + matigags) md of age 4-6 males with age 4-6 females (4 + x 4 + matings). Release group sizes were 7 1 943 and '93 742 fish for the 2 x 4+ and 4+ X 4+ groups, respectively. Observed returns of males (open bars) at ages 2-6 were 182, 74, 39, 6, and 0, respectively, for 2 x 4 + mzdtings and 12, 27, 8'9, 28, and 3, respectively, for 4 + x 4 + rnatings. Observed returns of females (solid bars) at ages 2-6 were 0, 23, 166. 36, and 0, respectively, for 2 x 4+ rnatings and 0, 13, 145, 32, md 2, respectively, for 4 + X 4 + matings.

at maturity were 0.9'7 yr for males and 0.78 yr for females. After adjustment for ocean fishery removals, differences between groups were 1.13 yr for males and 0.79 yr for females; after adjustment for ocean fishery removals and natural mortality, differences between groups were 1.05 yr for males and 0.8 1 yr for females.

Because the response to selection (difference in mean age of maturity between progeny groups) was little affected by adjustments for ocean fishery catches and natural mortality, calculated heritabilities for age of maturity were relatively insensitive to these same adjustments (Table 8). Calculated heritabilities ranged from 8.49 to 0.57 for males, from 8.39 to 0.4 1 for females, and from 0-49 to 0.54 for combined sexes.

Mean scale distances to annulus i for fish that returned to freshwater and matured at ages greater than i showed a consistent trend for younger-matwing fish to have lager scale measurements and hence larger size at age. For example, for

4 988 BROOD

1 2 3 4 5 6 7 AGE AT MATURITY

FIG. 4. Observed age- and sex-specific returns sf fdl chinook salmon to Elk River from 1980 brood year rnatings of age 2 males with age 4-6 females (2 x 4+ matings) and age 4-6 males with age 4-6 females (4 + X 4 + rnatings). Release group sizes were 105 084 and 114 528 fish for the 2 x 4+ and 4+ x 4+ groups, respectively. Observed returns of males (open bars) at ages 2-6 were 569, 140, 36, 4, and 0, respectively. for 2 x 4 + rnatings and 85,97, 132, 29, and 3, respectivejy , for 4 + x 4 + rnatings. Observed returns of females (solid bas) at ages 2-6 were 0. 59. 170, 4, and 1 , respectively, for 2 X 4 + matings and 0, 34, 184, '7 1 . and 2, respectively, for 4+ X 4+ rnatinys.

females that matured at ages 3, 4, and 5 from the 3 x 3 group, mean scale measurements to annulus 2 were 240.0, 230.6, and 220.0 ocular units, respectively; these mean scale measurements were 259.6, 23 B .6, and 230.8 ocular units, respectively, for females from the 5 x 5 group (Fig. 2). Within 3 x 3 and 5 x 5 groups, t-tests generally supported a conclusion that mean scale distances to annulus 2 for males and females that matured at age 3 were significantly greater than distances for fish that matured at age 4 or 5.

Although mean scale distances to annuli (Fig. 2) suppc~rt a contention that, within an experimental group, faster-growing fish tend to mature at an earlier age, they do not suggest that progeny h m the 3 x 3 group were, as a group, faster growing than progeny from the 5 x 5 group. Substitution of the hypothetical numbers of males and females destined to mature at ages 3-5 (Table 7) and the mean scale distances to annulus 2 for fish that maaatured at ages 3-5 into equation (2) produced

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3 x 3 Progeny 3 x 3 Progeny

5 x 5 Progeny

LENGTH LENGTH

5 x 5 Progeny 1--- I I I --

LENGTH LENGTH

I I I

' -7

FIG. 5. Two alternative hypotheses that might describe the connection between marine growth and age s f maturity in chinook salmon. For both alternatives, it is assumed that length distributions at age 2 are normal with equal variance. In Fig. 5A, it is assumed that progeny f s m 3 X 3 and 5 x 5 matings have equal minimum threshold size that triggers maturation (broken vertical line), but mean length sf 3 X 3 progeny exceeds mean length of 5 x 5 progeny. In Fig. 5B, it is assumed that progeny from 3 x 3 and 5 x 5 matings have equal mean length, but minimum threshold size is smaller for progeny from 3 x 3 matings. Hatched areas of distributions indicate progeny that mature at age.

approximate indices of mean cohort length at annulus 2 for the 3 X 3 and 5 X 5 experimental groups. Calculated mean cohort scale distances to annulus 2 were 232.7 and 235.19 ocular units for females from the 3 x 3 and 5 x 5 groups, respectively, and 24 1.4 and 241.8 ocular units for males from the 3 X 3 and 5 X 5 groups, respectively.

1979 and 1980 Brood Year Experiments

Observed river returns of males and females from 1979 and 1980 brood year 2 x 4 + and 4 + x 4 + groups suggested that age of male parent has little impact on age of maturity of female progeny (Fig. 3 and 4). For the 1979 and 1980 brood years, respectively, mean ages at maturity of male progeny from the 2 X 4 + groups were 2.56 and 2.30 yr whereas mean ages at maturity sf male progeny from the 4 + X 4 + group were 3.89 and 3.30 yr. In contrast, mean ages at maturity of females wre 4.06 and 3.98 yr for the 2 X 4 + groups and 4.12 a d 4.14yr for the 4+ x 4 + groups.

Discussion

Results from the age-specific mating experiments carried out with chinook salmon at Elk River Hatchery provide additional

evidence that age of parent has a strong influence on age of maturity of progeny. The most meaningful estimates of herit- ability from these experiments are probably those based on freshwater returns of mature progeny from the 1974 brood year, adjusted for ocean fishery interceptions of immature fish (i.e. hypothetical unexploited age composition of mature progeny, Table 6). These estimates, 0.57 and 0.40 for males and females, respectively, are similar to those reported by Gjerde ( 1 984) and Gjerde and Gjedrem (1984) for Atlantic salmon (Salrno salar) (0-39 for males and 0.48-8.49 for females) (see also Gjedrem 1985) and by Gall et al. (1988) for rainbow trout (Oncorhyn- chus mykiss) (0.38) (see also Tipping 1991). Iwamoto et al. (1984) found that tendency for males to mature as jacks was also strongly dependent on male parent age in coho salmon (Oncorhynchus kisutch), but it is not clear that their heritability estimates are directly comparable with those reported above.

However. as reported previously (Ellis and Noble 1961 ; Ricker 1972) and as indicated by returns from 1979 and 1980 brood year experiments in this study, age of male chinook salmon parent has little influence on age of maturity of female progeny. This finding from hatchery mating experiments is consistent with empirical observations of the age and sex csm- positions of natural spawning populations of chinook salmon.

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As noted in the introduction, some late-maturing populations (in which females mature primarily at age 5 ) produce substan- tial numbers sf jacks whereas some early-maturing populations (in which females mature primarily at ages 3 and 4) have rel- atively few jacks (Nicholas and Wankin 1988). It seems unlikely that such differences in jack maturation rates among spawning populations could be maintained if female parent age exerted a strong effect on male progeny age at maturity.

Unfortunately, because there were no reciprocal matings in which females of varied ages (e.g. ages 3 and 5) were mated with males of fixed age (e.g. age 2), it was not possible to determine the effect of female parent age on male progeny age of maturity, In this respect, the more sophisticated mating pro- tocols and linear statistical analysis models used by Gjerde (1984) and Iwamoto et al. (1984) provide useful guidance for future age-specific mating experiments with chinook salmon. In future experiments, it would also be desirable to mark prog- eny with CWTs rather than with fin clips. We adjusted fresh- water returns from the 3 x 3 and 5 x 5 groups for ocean fishery catches based on ocean fishery exploitation rates expe- rienced by CWT fish released at a similar date and size from the same brood year. Although these adjustments were reason- able, they cannot substitute for direct adjustment based on recoveries of fish released with CWTs. It is conceivable, for example, that fish destined to mature at different ages had dif- ferent mean distributions and were subject to different ocean fishery exploitation rates. If this were the case, then the adjust- ments for ocean fishery catches made in this paper may have produced misleading results.

Other possible improvements in the design of age-specific mating experiments for chinook salmon include tagging of progeny by family to allow separation of variation in progeny age of maturity due to within-parent and between-parent com- ponents; equalizing progeny numbers per female to equalize influence of individual females if fish are released with a single tag code; ensuring that individual males are mated with indi- vidual females in all cases; and contrasting month of release as well as parent age across groups to allow assessment of the interactions among parent age and progeny marine size at age and age at maturity. Hankin (1990) found large between-year variation in lengths of hatchery chinook salmon released in the same months, and he also found that age-specific maturation probabilities were positively correlated with mean length at maturity. Only carefully structured mating experiments could allow these important environmental influences on age of matu- rity to be separated from the effects of parent age. In view of published concerns regarding the potential repercussions of fishery-induced reduction in average ages of spawning chinook salmon, we find it surprising that so very few age-specific mat- ing experiments have been conducted. We are not aware of any more recent breeding experiments which have been designed to assess inheritance of age of maturity in chinook salmon.

Scale measurements from mature progeny from the 3 x 3 and 5 x 5 mating groups generally supported a long-standing contention that faster-growing chinook salmon mature at a younger age (Parker and Larkin 1959) and are consistent with Nielsen and Geen9s (1 986) finding that Sixes River, Oregon, chinook salmon that were lager at annulus 1 generally matured at earlier ages. Within mating groups, faster-gowing Elk River chinook salmon progeny generally matured at earlier ages (Fig. 2). Between-group compa~sons of calculated indices of mean cohort lengths, however, suggested that mean lengths at annulus 2 for male and female progeny from 5 x 5 matings (235 and 242 oculw units, respectively) were not less than mean

lengths at annulus 2 for male and female progeny from 3 x 3 matings (232 and 24.1 ocular units, respectively). Calculated mean cohort sizes may be negatively biased by exclusion of (faster-growing?) males that matured as age 2 jacks and by selective ocean fishery removal of faster-growing males and females at ages 2 and 3 (at which ages, almost all and some, respectively, chinook salmon are below legal size limits in commercial fisheries). These effects were probably relatively modest in these experiments, however, at least for females. At age 2, estimated annual ocean fishery exploitation rates for comparable 19'74 brood year CWT chinook salmon released from Elk River Hatchery were only about 0.005, and no females matured at this age. Even at age 3, estimated ocean fishery exploitation rate was relatively modest (8.2 1) for 1974 brood year Elk River fall chinook salmon.

The above finding of no apparent between-group differences in indices of mean length at annulus 2, and %warnoto et al.'s (1984) related finding that full-sib groups of coho salmon with higher percentages of jack maturation did not grow at signifi- cantly faster rates than other groups, suggest that inheritance of age of maturity in chinook salmon cannot be a direct and simple reflection of inheritance of growth rate. Instead, some additional inherited factor that is not tightly associated with growth rate must also influence age of maturity (see also Alm 1949, 1959; Gardner 1976). We speculate that such an inherited factor can be represented by age- and sex-specific minimum threshold sizes that may trigger differentially maturation at age.

For the sake of argument and to motivate our perferred hypothesis, we assume that lengths at annulus 2 of chinook salmon progeny from the 3 x 3 and 5 x 5 mating groups were normally distributed with equal variance. We present two alter- native hypotheses regarding the connections among maturation at age 2 (naales) or 3 (females), threshold lengths, and length at age. In the first alternative, we assume that 3 x 3 progeny are faster growing than 5 x 5 progeny, but progeny from both groups share common minimum threeshold sizes that trigger maturation by sex at age (Fig. 5A). In this case, a greater pro- portion of 3 X 3 progeny should mature (at age 2 for males or at age 3 for females) and the average length at maturity should be longer for 3 x 3 progeny than for 5 x 5 progeny. For the second alternative, we assume that progeny from the 3 x 3 and 5 x 5 matings have a common mean and variance of length at age 2, but minimum tkreshoid lengths that trigger maturation by sex and age are shorter for progeny from 3 x 3 parents than from 5 x 5 parents (Fig. 5B). In this case, one would expect that greater proportions of male and female progeny from the 3 x 3 group would mature at ages 2 and 3, respectively, as compared with the 5 x 5 group, and average lengths at matu- rity should be shorter for mature progeny from the 3 x 3 group as compared with the 5 x 5 group.

Results from the 1974 experiment appear more consistent with the second alternative hypothesis than with the first. Both alternatives correctly predict that a larger fraction of a cohort should mature at earlier ages among 3 x 3 progeny than among 5 X 5 progeny, and both alternatives correctly predict that faster-growing progeny within a given mating group should mature earlier than slower-growing progeny. Also, the exist- ence of a hypothetical minimum threshold size for maturation is supported by hatchery month of release experiments which show that size at age has an important influence on age 2 matur- ation probability of male Trinity River, California, chinook salmon, which increases dramatically once fish exceed about 46 cm (Hankin 1990, fig. 2). As mentioned previously, how- ever, calculated indices of mean length at age 2 are more

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consistent with an hypothesis that groups had equal mean and variance at age 2 than with an hypothesis that mean length of 3 x 3 progeny exceeded that of 5 X 5 progeny.

Mean sizes of mature progeny from the 3 x 3 and 5 X 5 mating groups also appear more consistent with the second hypothesis than with the first. At ages 2 and 3, mean MEPS lengths of mature males (see Table 4) from the 5 x 5 group (406.4 and 64 1 .O mm, respectively) were significantly larger than mean MEPS lengths of mature males from the 3 x 3 group (395.6 and 617.9 mm, respectively) ( t ' = 17.2 and 6.623, respectively, for comparisons of means at ages 2 and 3; Sne- decor and Cochran 1967, p. 1 15). Among females, for which mean RI[EPS lengths of mame age 3 females were 639.7 and 633.1 mm for the 3 x 3 and 5 x 5 groups, respectively, there was no significant difference in mean lengths between groups, a result inconsistent with both alternative hypotheses. The small sample size for age 3 females from the 5 x 5 group (n = 181, however, limited the power of this comparison. On balance, results from these experiments thus appear to support a tentative hypothesis that minimum threshold sizes that trigger maturation at age are shorter for progeny of younger parents (Fig. 5B).

Finally, we wish to add our brief thoughts to those of others who have commented on the potential significance of reduction in the mean size and age of spawning salmon for management of wild and hatchery salmon stocks. The extreme future sce- narios sketched by Wicker (1980, p. 18) for wild populations - d l females spawn at age 3 and all males at age 2, or stocks might be lost because young spawners cannot cope adequately with their reproductive environment - assume that calculated single-trait heritabilities may be validly used to determine potential genetic selection by fisheries. For a variety of reasons, Riddell (1986) argued that calculations based on single-trait heritabilities may greatly exaggerate the potential genetic effects of fisheries on age of maturation of wild (Atlantic) salmon pop- ulations. Wicker's calculations also did not acknowledge the potential importance of reproductive behavior of chinook salmon. Older and larger male chinook salmon appear to have much greater success than smaller and younger males in com- peting for female mates in wild spawning populations (Baxter 199 1). Natural spawning behaviors in wild populations may thus help buffer the potential fishery-induced genetic selection toward younger age of maturity, at least among males.

Rickerqs (1980) extreme scenarios based on single-trait her- itability calculations may have substantial relevance for hatch- ery stocks of chinook salmon, however. In contrast with wild populations, hatchery chinook salmon released as subyearling smolts in fall exhibit little variation in juvenile life history that may affect age of maturity; variation in smolt size is greatly reduced when compared with wild smolts; levels of early life mortality are much lower than for wild populations; almost all eggs from females survive to be released, regardless of egg size or female size; and reproductive behaviors of adults that may favor larger and older fish spawning naturally are irrelevant in the hatchery spawning environment. If younger chinook salmon were spawned at random in hatcheries, without regard to age or size, then substantial (unintentional) selection for young age of maturity and resultant loss of genetic diversity should result.

For the above reasons, Oregon's recently adopted Coastal Chinook Salmon Plan (ODFW 1991) calls for implementation of hatchery spawning guidelines for chinook salmon that gen- erally favor higher ages of both sexes. Specifically, guidelines require that (a) almost all females will be mated with males of equal or larger size (jacks would be used in no more than one out of every ten matings) and (b) proportions of age 3 females

used for spawnings will be reduced to roughly half the propor- tions of age 3 females that are found in spawning runs. Actual proportions of age 3 females spawned will be tailored to indi- vidual stocks according to their "natural" maturity schedule, with greater proportions spawned in early-maturing stock types than in late-maturing stock types. Although these guidelines are preliminary rand rather general, we believe that implementation of these guidelines should provide reasonable protection against unintentional selection for young age of maturity among hatch- ery stocks of chinook salmon.

Acknowledgments

Paul Reimers was largely responsible for initiating the age-specific mating experiments with chinook salmon at Elk River Hatchery. We acknowledge Paul's vision and his concern for the potential impacts of hatchery practices on wild populations of chinook salmon. We thank K* Johnson, Pacific Marine Fisheries Commission, for ocean recovery data for CWT chinook salmon released from Elk River Hatchery, Lisa Borgerson and Roy Beatty for assistance with scale reading and scale measurement, and an anonymous referee for useful revision sugges- tions. Partial support for the senior author's efforts was provided by the Oregon Department of Fish and Wildlife for which special thanks are due Jim Lichatowich.

References

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1959. Connection between maturity, size, and age in fishes. Rep. Inst. Freshwater Res. Dmttningholm 46): 5-145.

BAXTER, R. D. 1991. Chinook salmon spawning behavior: evidence for size- dependent male spawning success and female mate choice. M . S . thesis, Humboldt State University, Arcata, CA. 115 p.

BEACHAM, T. D., AND C. B . MURRAY. 1990. Temperature, egg size, and devel- opment of embryos and alevins of five species of Pacific salmon: a com- parative analysis. Trans. Am. Fish. Soc. 119: 927-945.

CHILTON, B. E., AND H. T. BBLTON. 1986. New method for ageing chinook salmon (Q~tcorhj~nchers €sha~)ybcha) using dorsal fin rays, and evidence of its validity. Can. J. Fish. Aquatat. Sci. 43: 1588-1594.

CLEAVER, F. C. 1969. Effects of ocean fishing on 1961-bmd fa11 chinook salmon from Columbia River hatcheries. Res. Rep. Fish Comm. Oreg. I: 3-76.

DONALDSON, L. W. , AND K. BONKAM. 1970. Effects of chronic exposure of chinook salmon eggs and alevins to gamma radiation. Trans. Am. Fish. SOC. 99: 112-1 19.

~ONALDSON, L. R., AND D. MENASVETA. 1961. Selective breeding of chinook salmon. Trans. Am. Fish. Soc. 90: 160-164.

ELLIS, C. H., AND R. E. NOBLE. 196Q. Marked fish returns. Returns of marked fall chinook salmon to the Beschutes River. Wash. Bep. Fish. Annu. Rep. 1959, 69: 44-47.

1961. Returns of marked fall chinook salmon to the Deschutes River. Deschutes River genetics experiment. Wash. Dep. Fish. Annu. Rep. 1960, 70: 72-75.

FALCONER, D. S. 1981. Introduction to quantitative genetics. 2nd Ed. Long- man, London. 340 p.

GALI,, G. A. E., J . BALTODANO, AND N. HUANG. 1988. Heritability of age at spawning for rainbow trout. Aquaculture 68: 93-102.

GARDNER, M. L. G. 1976. A review of factors which may influence the sea- age and maturation of Atlantic salmon Saimo satar. L. 3. Fish. Biol. 9: 289-327.

GHARRETT, A. J . , AND S. M. SHIRLEY. 1985. A genetic examination of spawn- ing methodology in a salmon hatchery. Aquaculture 47: 245-256.

GJEDREM, T. 1985. Genetic variation in age at maturity and its relation to growth rate, p. 52-61. In R. M. Iwamoto and S. Sower [ed. j Salmonid reproduction: an international symposium. b'ashington Sea Grant, Seat- tle, WA.

GIERDE, B. 1984. Response to individual selection for age at sexual maturity in Atlatnic salmon. Aquaculture 38: 229-240.

GIEWDE, B., AND T. GJEDREM. 1984. Estimates of phenotypic and genetic parameters for carcass traits in Atlatnic salmon and rainbow trout. Aqua- culture 36: 97-1 10.

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