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Oct 21, 2009 - Abstract All other things being equal, the lifetime repro- ductive success (LRS) of iteroparous and semelparous individuals should scale with ...
Behav Ecol Sociobiol (2010) 64:505–513 DOI 10.1007/s00265-009-0866-7

ORIGINAL PAPER

Sex-specific patterns of lifetime reproductive success in single and repeat breeding steelhead trout (Oncorhynchus mykiss) Todd R. Seamons & Thomas P. Quinn

Received: 9 December 2008 / Revised: 16 September 2009 / Accepted: 17 September 2009 / Published online: 21 October 2009 # Springer-Verlag 2009

Abstract All other things being equal, the lifetime reproductive success (LRS) of iteroparous and semelparous individuals should scale with the number of breeding seasons. Deviations from this relationship may occur for many reasons, including age- or size-related fecundity or life history trade-offs, which may differ between sexes. We used 19 brood years of DNA parentage analysis in a small (N=4–143 year−1) wild, unexploited population of steelhead trout (Oncorhynchus mykiss) to compare the LRS of individuals that spawned only once [“one time spawners” (OTS), N=355 male, 371 female] to those spawning twice [“repeat spawners” (RPS), N=13 male, 49 female]. Female RPS had nearly twice the LRS of female OTS (1.17 offspring per female vs 0.91 offspring per female), whereas male RPS had nearly three times the LRS of male OTS (1.54 offspring per male vs 0.57 offspring per male). Female RPS produced slightly more adult offspring during their second breeding season than their first (0.78 vs 0.82 offspring per female); however, male RPS produced all of their adult offspring in their second breeding season (0 vs 1.54 offspring per male). The additional growth in body size of males between breeding seasons may give them an advantage in their second breeding season, but the lack of offspring produced in their first season suggests a trade-off

Communicated by K. Lindström Electronic supplementary material The online version of this article (doi:10.1007/s00265-009-0866-7) contains supplementary material, which is available to authorized users. T. R. Seamons (*) : T. P. Quinn School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA 98195, USA e-mail: [email protected]

between survival and future reproduction that was not expressed in females. Keywords Iteroparity . Life history . Lifetime reproductive success . Parentage assignment . Scale analysis . Semelparity

Introduction For a semelparous species, since all reproduction occurs in one single bout, reproductive success is almost entirely dependent on producing as many offspring as possible. For iteroparous species, the most important factor determining individual lifetime reproductive success (LRS) is survival between bouts of breeding (e.g., Gaillard et al. 2000). The simultaneous need to both survive and maximize reproductive success leads to the possibility of life history trade-offs (Stearns 1992). All other things being equal, iteroparous individuals should produce as many more times the number of offspring of semelparous individuals as they have breeding seasons. However, because of energetic and other constraints on both survival and reproductive success, all things are not equal. The LRS may be higher than expected for iteroparous individuals because they become better parents later in life, for example, producing higher quality offspring (Marteinsdottir and Steinarsson 1998) or by providing better parental care (Weladji et al. 2006). Because growth often occurs between breeding seasons, organisms whose fecundity is related to body size (e.g., fishes, Beacham and Murray 1993) may also produce more offspring per individual as they age. Alternatively, the LRS of older iteroparous individuals may be lower than expected because of reproductive senescence (Espie et al. 2000). This type of deviation may also occur because of an evolutionary life history trade-off between energy investment in current

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and future reproduction (or current reproduction and survival to breed again, Stearns 1992). If semelparous individuals invest more energy in what is their only attempt at breeding, they may have relatively higher reproductive success, causing the LRS of iteroparous individuals to be lower than expected. Patterns of reproductive success in fishes may be very different than that of other organisms. Unlike birds and mammals, fishes generally have indeterminate growth and strong size-dependent fecundities (Hendry et al. 2001). Thus, older fishes are expected to produce significantly more offspring than younger, smaller fishes. Some fishes are very long lived [>100 years, e.g., sturgeons (Acipenser spp.) or rockfishes (Sebastes spp.)] and could thus produce many million more offspring than younger fishes. Older, larger fish may also produce larger or higher quality eggs (Beacham and Murray 1993; Berkeley et al. 2004; Quinn et al. 1995), and larger fish may provide a better rearing environment (Lapointe et al. 2000; Steen and Quinn 1999) or guard the young better than smaller fish (Fleming and Gross 1994). However, measuring reproductive success in most fish is difficult, mainly due to difficulties in sampling complete or near-complete breeding populations. In addition, many empirical studies of age and reproductive success have been limited by reliance on an early life history stage of the offspring as the measure of reproductive success (Forslund and Part 1995), and patterns may be different when reproductive success is measured by adult offspring (Espie et al. 2000; Roff 1981). Our overarching goal has been to study individual LRS and fitness in a wild, natural population of steelhead trout (Oncorhynchus mykiss). Salmonid species and populations span the range of the semelparity–iteroparity continuum, from fully semelparous Pacific salmon (Oncorhynchus spp.) to iteroparous trout and charr (Oncorhynchus spp., Salmo spp., Salvelinus spp.). Steelhead are technically an iteroparous species, but most individuals do not survive to spawn a second time (and so are functionally semelparous), and very few spawn three or more times (Busby et al. 1996). They share not only some life history characteristics of their semelparous congeners, most notably anadromy with an extended ocean feeding migration, thought to be a necessary component for the evolution of semelparity (Crespi and Teo 2002), but also exist as completely nonanadromous populations (rainbow trout), which have comparable life histories with other non-anadromous, iteroparous salmonid species. Furthermore, steelhead are phylogenetically closest to the semelparous salmon (Oakley and Phillips 1999), which currently exist in sympatry with most of the semelparous salmon and likely evolved under the same conditions. Therefore, we posed and answered the following questions: (1) Do steelhead that spawn more than once (iteroparous individuals) have more offspring than

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those that spawn only once (semelparous individuals)? (2) Do iteroparous individuals produce more offspring in their second breeding season than in their first, and is there a different pattern for males and females? To increase chances of survival, iteroparous individuals may invest less in their first breeding season than semelparous individuals invest in their only breeding season; thus, finally, we asked, (3) Do semelparous individuals produce more or fewer offspring than iteroparous individuals in their first breeding season?

Methods Sampling site and sample collections Our research was performed in Snow Creek, one of the two small creeks that flow directly into saltwater at Discovery Bay in Washington State, USA. Steelhead spawn in both creeks, but Salmon Creek has less available spawning and rearing habitat and a much smaller steelhead population than Snow Creek (see map in Seamons et al. 2004b). Adult steelhead were captured in Snow Creek by employees of the Washington Department of Fish and Wildlife (WDFW). The Snow Creek steelhead population is maintained for research and monitoring purposes, so there is no hatchery supplementation. Directed fishing is prohibited, and the return timing and location of the population make it unlikely that there are significant interceptions elsewhere, so this is essentially a fully wild, unexploited population. Fish were captured at a permanent weir that blocks their upstream spawning migration or occasionally by electrofishing below the weir. All upstream migrating adults were captured and measured for fork length, sex, and capture date were recorded, scales were taken for age analysis, and a small hole was punched in one operculum to confirm that the fish had been sampled prior to release above the weir. Every effort was made to sample all fish spawning above the weir but under conditions of heavy flooding some fish ascended without being sampled. The weir also traps downstream migrants, and any unmarked adults captured migrating downstream were sampled as described above. Analysis of scales was performed by employees of WDFW. Tissues used for DNA analysis included scales or fin clips from brood years 1982 through 2004. Scales had been dried and stored in envelopes. From 1997 to 2004, fin tissue samples were taken in addition to scales and stored in 95% ethanol for DNA analysis. Identification of repeat spawning fish More female than male steelhead survive to spawn more than once, and repeat spawning steelhead may spend 1 or

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2 years in the ocean between spawning migrations (Burgner et al. 1992). Repeat spawning steelhead were identified in two ways: by the presence of a “spawning check” on fish scales (Davis and Light 1985; Persson et al. 1995) or by the presence of identical individual genotypes in consecutive brood years (see below). Available individual phenotypic data (healed operculum scar, age, sex, length, and brood year) were used to validate the identification of RPS. As a measure of statistical confidence in genetically identified RPS, we calculated the probability of identity, an estimate of the probability of drawing two identical genotypes from the population at random (PID, Taberlet and Luikart 1999) for all loci with brood years pooled.

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the fish. Some repeat spawning individuals were only sampled in one of the brood years in which they spawned. In the absence of any other data, the year that the offspring of these fish was produced was ambiguous, i.e., it could have been produced the first or the second year the parent spawned. However, it was relatively straightforward to identify the years in which their offspring were produced (if detected) when other data were available. Offspring with ambiguous brood year determination were excluded from analysis (females, six offspring; males, one offspring). Further details of our sampling and laboratory methods may be found in (Seamons et al. 2004a, b, 2007). Statistical analysis

Molecular analysis and parentage assignment We first tested for differences in average LRS between sexes and parity levels (iteroparous RPS and semelparous OTS) using a two-way ANOVA. Offspring numbers of male and female RPS and OTS were not normally distributed (Fig. 1), so LRS was rank transformed (Zar 1999). If significant differences were detected in these tests, we then tested the null hypothesis that the reproductive success of RPS was only twice that of OTS. Values of reproductive success of OTS were doubled, and the LRS of OTS and RPS were rank transformed and tested for differences among groups using two-way ANOVA. We next tested for differences between 0.80

a)

0.70

Females

0.60

1 spawning season - OTS 2 spawning seasons - RPS

0.50 0.40 0.30 0.20 0.10 Proportion

DNA was extracted from scales and fin clips using Qiagen DNeasy Tissue 96-well extraction kits (Qiagen Inc., Valencia, CA, USA) following the manufacturer’s guidelines. Polymerase chain reactions (PCR) to amplify 12 microsatellite loci were performed (see Electronic supplemental appendix Table A1 for loci and PCR conditions), and alleles were visualized and size fractionated on a MegaBACE 1000 capillary DNA sequencer. Genetic data were tested for deviations from expected Hardy–Weinberg proportions with a two-tailed test using the Markov Chain method implemented in Genepop v3.4 (Raymond and Rousset 1995). Observed and expected values of heterozygosity and FIS were also calculated using Genepop v3.4. Global and locus-specific exclusion probabilities were calculated per brood year using Cervus 2.0 (Marshall et al. 1998). All adults that were captured and sampled in Snow Creek were used as potential parents. Parents were assigned to individual adult offspring using the principles of exclusion. That is, only adults that shared at least one allele at each locus with the putative offspring were called the true parents, and they had to match the opposite allele at each locus. All nonmatching adults were excluded as parents. If all adults were excluded from parentage, it was assumed that the true parents had not been sampled. No accommodation was made for genotyping or other errors. In some cases, all adults except one were genetically excluded as parents, and we concluded that one but not both parents had been sampled. The chance of matching a single parent is higher than matching two parents simultaneously (Marshall et al. 1998). As a measure of the veracity of these single-parent assignments, we calculated the probability of a random match of a single parent using equation 1 in Seamons et al. (2004a). By the combination of opercle punch, indicating that the fish in question had spawned, the DNA parentage data, and age as indicated from analysis of the scale samples, we were able to reconstruct the breeding histories of most of

0.00 0 0.80

1

2

3

4

5

6

b)

0.70

7

8

Males

0.60 0.50 0.40 0.30 0.20 0.10 0.00 0

1

2 3 4 5 6 # spawning adult offspring

7

8

Fig. 1 Lifetime reproductive success (proportion) of adult female (a) and male (b) steelhead that spawned in only one (OTS, gray bars) or at least two (RPS, white bars) seasons. Data are pooled from 19 brood years

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sexes and parity levels in LRS of OTS and the reproductive success of RPS in their first breeding season with a two-way ANOVA with LRS data rank transformed. Finally, we compared the reproductive success of RPS in their first and second breeding seasons using a Wilcoxon paired sample test. The data were taken from 19 brood years. Because there was no detectable difference in numbers of repeat spawning fish among years (randomization test, P= 0.15 females, P=0.13 males), the fish were pooled among all sample years for this analysis. All F statistics were calculated for two-tailed tests with α=0.05. Reproductive behavior (Quinn 2005), post-spawning survival, and repeat spawning rates (Burgner et al. 1992) typically differ between male and female steelhead. We tested for differences in the number of male and female OTS and RPS using a χ2 contingency table. We finally tested for differences between the sexes in the breeding seasons in which RPS fish produced their offspring using a χ2 contingency table. The vast majority of RPS fish spawned twice; only ten females and three males spawned more than twice. These samples were too small for statistical analysis, so offspring produced in the third and fourth breeding seasons by these individuals were excluded from all analyses to standardize RPS at two spawning seasons. All 13 RPS males failed to produce offspring in their first spawning season (see Results). Because the majority of males in this population failed to produce any detected offspring (> 70%, Fig. 1) and the number of repeat spawning males was low (N=13), we performed a post hoc re-sampling exercise to estimate the chances of randomly drawing 13 males with zero reproductive success. We drew 10,000 replicate samples of 13 males from the entire set of OTS and RPS male steelhead, with replace-

ment and with the LRS of all 13 RPS males set to zero. We then calculated the average LRS of each sample and examined the distribution of average LRS of 13 randomly drawn males. An average >0 indicated that at least one of the males drawn in a sample had an LRS >0.

Results Identification of repeat spawning fish A total of 921 adult fish were sampled between 1982 and 2000 (Table 1 of Seamons et al. 2007). Some of those fish were the same fish sampled in different years (i.e., RPS), so 834 different adults were sampled. A total of 8.3% (69) of the adults in the parental pool were identified as RPS from the presence of a spawning check on the scale sample (Table 1). Of those, 37.6% (26 of 69) were also genetically identified as repeat spawning individuals (observed PID = 6.6×10−5). Fish with identical genotypes were highly likely to be the same fish (unbiased PID =4.0×10−23, PIDsibs =5.6× 10−7). The other 43 fish identified by scale analysis as repeat spawning fish were captured in only one of their spawning migrations and so could not be verified by genetic data. Molecular analysis and parentage assignment Our genetic dataset was sufficient for accurate and powerful parentage assignment. Genotyping error was low (0.6% 3%, Seamons et al. 2004a), and heterozygosities among loci and brood years were generally quite large (average= 0.88, see Electronic supplemental appendix Table A2). The global exclusion probability among all brood years and loci

Table 1 The number of adult steelhead of each sex that exhibited a certain number of spawning seasons and their lifetime reproductive success (LRS) measured as spawning adult offspring

Female

Male

Total

N LRS LRS/N N LRS LRS/N N

All adults

Repeat spawning adults

Number of spawning seasons

Spawning season number

1

2

3

4

371 339 0.91 355 201 0.57 726

39 75 1.92 11 15 1.36 50

9 14 1.56 2 5 2.50 11

1 0 0 0 NA NA 1

1

2 49 38a 0.78 13 0 0.00

49 40a 0.82 13 20 1.54

Fish that spawned in any category of spawning seasons are not included in the total for fish that spawned in fewer or more seasons. Also shown is the lifetime reproductive success of fish that spawned at least twice in their lifetimes, broken down into the spawning season in which the offspring were produced a

Uncertain aged offspring omitted

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509 Table 2 The number of adult steelhead that produced their spawning adult offspring (lifetime reproductive success) in their first, second, or both first and second spawning season and those that returned to spawn in multiple years but failed to produce any spawning adult offspring

Statistical analysis of reproductive success

Female

Nearly equal numbers of males and females spawned once (N=355 and 371, respectively, Table 1), but more females than males survived to breed more than once (N=49 and 13, respectively, χ20:05; 2 =17.9, P=0.00013, Table 1) and a single female had the largest lifetime number of breeding seasons (four, Table 1). The total number of offspring produced by all female OTS was nearly four times as large as that of all female RPS, and all male OTS produced almost nine times as many offspring as all male RPS in their lifetime (Table 1). LRS was highly skewed for both OTS and RPS males and females; many individuals had no detected adult offspring and a few individuals had many offspring (Fig. 1). The proportion of male and female RPS having zero detected offspring was lower than that of male and female OTS, though the difference was significant only for females (females, χ20:05; 1 =8.97, P=0.005; males, χ20:05; 1 =3.79, P=0.10). Repeat spawning adults had higher LRS than fish that spawned only once (Table 1 and Fig. 2; F1, 784 =13.602, P=0.0002). On average, female RPS had 1.9 times the

Male

Average number of spawning adult offspring (lifetime reproductive success)

was 1.00 for both parents. At least one parent was assigned to 65.7% (494) of all returning adults. Of these fish, 36.8% (182) were assigned both parents, 53.2% (263) were assigned only a mother, and 9.9% (49) were assigned only a father (Seamons et al. 2007). Our single parent assignments were robust, having an average probability of a random match of 0.002. For a more detailed report on our genetic data and parentage, see Seamons et al. (2007).

1.6

Daughters 1.4

Sons

1.2 1.0 0.8 0.6 0.4 0.2 0.0 OTS

RPS

Males

OTS

RPS

Females

Fig. 2 Average number of spawning adult daughters (gray bars) and sons (white bars; ±1 SE) for adults that spawned only once (OTS) or at least twice (RPS) in their lifetime. Repeat spawning female and male steelhead produced more spawning adult offspring than adults that spawned only once in their lifetime (t tests, female P=0.09, male P=0.006)

Spawning season of RPS when offspring were produced 1 N % N %

2 10 20.4 0 0.0

12 24.5 7 53.8

1 and 2

Neither

9 18.4 0 0.0

18 36.7 6 46.2

reproductive success of OTS females, while male RPS produced nearly 2.7 times the number of adult offspring as OTS males. There was no difference in LRS between male and female steelhead (F1,784 = 1.935, P= 0.165), and there was no significant interaction of sex and parity (F1,784 =0.063, P=0.802). Repeat spawning adults also had LRS more than twice that of OTS (F1,784 =4.768, P=0.029). There was no difference in LRS of RPS and twice the LRS of OTS between male and female steelhead (F1,784 =1.626, P=0.203), and there was no significant interaction of sex and parity (F1,784 =0.152, P=0.696). The spawning seasons in which male and female RPS produced offspring differed (Table 2, χ20:05; 1 =8.165, P= 0.042). Most female RPS failed to produce any adult offspring (18 out of 49, Table 2). Of those that were successful, most produced their offspring in the first or the second breeding season rather than both (22 out of 31, Table 2). Although the average number of offspring produced by female RPS in their second breeding season was slightly higher than that produced from their first breeding season, the difference was not significant [Fig. 3, Z0.05(2),49 =−0.258, P=0.80]. About half (N=6) of all male RPS failed to produce any offspring in their lifetime (Table 2). Surprisingly, those that were successful produced all of their detected offspring from their second breeding season [Fig. 3, Z0.05(2),13 =-2.379, P=0.017]. Thus, they had nearly three times the success during their second reproductive season as male OTS had in their only season. The reproductive success of RPS adults in their first season was less than that of OTS in their only breeding season (average=0.61 vs. 0.74, respectively; F1, 784 =4.000, P= 0.046) and differed between the sexes (male average=0.55, female average=0.90; F1, 784 =10.994, P=0.001; interaction of sex and parity was not significant, F1,784 =2.717, P=0.100). The chance of randomly drawing 13 males with average LRS=0 was very small (146/10,000). Any increase in reproductive success in the second breeding season may have been because RPS fish had

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Average number of spawning adult offspring (lifetime reproductive success)

510 1.6

Daughters 1.4

Sons

1.2 1.0 0.8 0.6 0.4 0.2

0

0.0 1st

2nd

Males

1st

2nd

Females

Fig. 3 Average number of spawning adult daughters (gray bars) and sons (white bars; ±1 SE) produced in either the first (1st) or second (2nd) spawning season of adult steelhead that spawned at least twice in their lifetime. Repeat spawning male steelhead apparently failed to produce any offspring from their 1st spawning season as no spawning adult offspring were detected. There was no difference in the number of spawning adult offspring produced by female steelhead in their 1st or 2nd spawning season (daughters and sons pooled, paired t test, P=0.87). The difference in numbers of spawning adult offspring produced by male steelhead was statistically significant (daughters and sons pooled, paired t test, P=0.01)

grown and so could produce more eggs or be competitively superior. We had length measurements in first and second breeding seasons for a subset of our RPS adults. Female RPS grew an average of 41 mm between their first and second breeding seasons (SD=15, n=16), and male RPS grew an average of 71 mm (SD=20, n=3). We estimated that female growth resulted in an average increase in fecundity of ∼400 eggs, or about 10% [fecundity=0.069 (length)1.661; Thom Johnson, WDFW, personal communication]. Thus, the increase in fecundity may largely explain the difference in average reproductive success of females.

Discussion Repeat spawning (i.e., iteroparous; RPS) steelhead produced more than twice the number of offspring in their lifetime than fish that spawned only once in their lifetime (i.e., semelparous, OTS; Fig. 2). All other things being equal, iteroparous individuals that spawned twice in their lifetime would have produced only twice as many offspring as semelparous individuals. The reproductive success of iteroparous individuals might be less than twice that of semelparous individuals if an energetic trade-off between reproductive success and survival existed. Alternatively, advantages conferred on repeat breeding individuals in later breeding seasons (e.g., increasing fecundity with age,

DelGiudice et al. 2007; Sparkman et al. 2007) might cause reproductive success to be more than twice that of semelparous individuals. Here, iteroparous female steelhead showed some growth between breeding seasons, and larger females (regardless of parity) often had higher reproductive success (Seamons et al. 2007), though iteroparous female steelhead in their second breeding season may be smaller for their age than virgin females of the same total age (age three females, TRS, unpublished data, Atlantic salmon, Salmo salar, Schaffer and Elson 1975). Iteroparous female steelhead produced more offspring (mainly daughters) in their second breeding season than their first (Fig. 3), and the number of females producing offspring was slightly higher in the second season than the first season (Table 2). The gain in reproductive success in the second breeding season may be accounted for by an increase in fecundity (about 10%) associated with the small amount of growth between seasons, though we cannot rule out other processes contributing to the difference. Iteroparous males, on the other hand, appeared to have a clear advantage in their second breeding season, producing more than twice as many offspring as OTS males produced (Fig. 2). Intriguingly, RPS males produced all their offspring in their second breeding season (Fig. 3). The fact that anadromous repeat spawning male steelhead failed to produce a single offspring from their first breeding season, combined with apparently substantial growth between spawning seasons, may be explained by an evolutionary trade-off between current reproduction and survival. Male salmon and trout compete for access to females during spawning, creating a dominance hierarchy (Quinn 2005). The physical competition among males is energetically taxing (Jonsson et al. 1997) and often results in physical injury. The migration from the ocean to home is also energetically taxing (in sockeye salmon, Oncorhynchus nerka, Hendry and Berg 1999), so why might a male make the journey then fail to spawn? Because size at age and age at maturity vary, there is no way for maturing fish to have a priori knowledge of their relative size on the spawning grounds, and it is relative size that determines reproductive success (Lande and Arnold 1983; Seamons et al. 2007). Larger males tend to hold higher, more favorable positions in the dominance hierarchy during mating (e.g., Dickerson et al. 2002; Quinn and Foote 1994). However, postbreeding survival was higher for smaller Atlantic salmon, another iteroparous anadromous salmonid species (Jonsson et al. 1991). We hypothesize that, when male steelhead arrive on the spawning grounds, they pursue one of two strategies. Some stay for months and compete for access to females, depleting their energy and reducing the probability of spawning in future years. This may be the most successful strategy for largest males. Other males may minimize their involvement in the current breeding event,

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conserve energy, and increase their chances of surviving to spawn again by quickly returning to sea to grow larger for the next breeding season. This strategy may be most successful for smaller males. Korman et al. (2007) reported that male steelhead spent more time on the spawning grounds than females, suggesting that males are not making such decisions but are simply maximizing reproductive success through opportunity. On the other hand, our own unpublished data show that, on average, males spent 1 day less on the spawning grounds than females (48 vs. 49 days) but ranged between 2 and 144 days (SD=19 days, females; range, 1–255, SD=28). Males that spend very little time on the spawning grounds may be the ones that fail to reproduce successfully their first breeding season but are more likely to survive to return and reproduce in the future. Unfortunately, we cannot test this hypothesis because we do not have the data to link duration on the breeding grounds, survival between spawning, and LRS. Steelhead are considered an iteroparous species; however, most steelhead spawn only once in their lifetime, and of the few that spawn more than once, most spawn only twice (Busby et al. 1996). Steelhead are more closely related to the semelparous Pacific salmon than they are to the other iteroparous salmonid species (Oakley and Phillips 1999). Though they share many life history traits with the semelparous salmon, including anadromy and long-distance ocean migration, many behaviors and life history traits are more in common with other iteroparous salmonids, including a more prolonged stay in freshwater as juveniles and a lack of nest defense behavior in females as adults (Quinn 2005). Charnov and Schaffer (1973) pointed out that the evolution of parity is linked to the survival of young offspring relative to that of survival of adults between bouts of breeding. We do not have rigorous estimates of the survival of adults between years of spawning; however, the numbers of repeat spawning adults are fewer in the years comprising this study (1982–2000) than in the years prior (1977–1981; WDFW, unpublished data). The genetic control, if any, of parity in steelhead is unknown. Assuming some genetic control and assuming offspring survival has not changed, fitness of the iteroparous may have been higher in the past. Obviously, both life history types (genetic or not) were present in the population. Selection on adult length and migration timing varied in magnitude, direction, and shape in this population (Seamons et al. 2007), and it is likely that the fitness of each life history type likely shifted as juvenile and adult survival changes with variable environmental pressures. Although annual variation in survival was not captured in our study, our main conclusions were robust to the decrease in sensitivity due to pooling data across years. A major difficulty of empirically measuring evolutionary fitness of parity is that semelparity is the default life history phenotype. That is, if an individual is genetically disposed

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toward iteroparity but failed to survive to spawn a second time, it would be classified as semelparous. If there were significant differences in investment in reproduction between semelparous individuals and iteroparous individuals in their first breeding season, the inclusion of a number of semelparous-appearing iteroparous individuals would artificially lower the mean reproductive output of the semelparous group and increase the differences between the groups. This would be most apparent in our data from male steelhead, and adjusting for it would diminish the differences between the groups. In spite of these limitations, the fact that iteroparous male steelhead produced no offspring their first breeding season is still quite interesting. Male salmonids are known for their variable breeding strategies and tactics (Quinn 2005), for example, precocial non-anadromous maturation (Koseki and Maekawa 2000; Morán et al. 1996; Seamons et al. 2004b). Indeed, precocially mature males played a significant role in our population, likely accounting for the relatively stable effective population size to census size ratio (Ardren and Kapuscinski 2003) and the difference in average reproductive success between adult females and (large, anadromous) males (Seamons et al. 2004b, 2007). Precociously mature males of many iteroparous salmonid species are known to be iteroparous (e.g., Atlantic salmon, Myers 1984); however, nothing is known about the parity of precocious male steelhead. Further research may reveal new strategies for iteroparous, anadromous salmonids. Demographic implications In addition to the implications of our data for the life history of this species, the data are also relevant to the conservation of this population and ones like it. Snow Creek steelhead, a member of the Puget Sound Evolutionarily Significant Unit recently listed as “threatened” under the US Endangered Species Act (http://www.nwr.noaa.gov/ESA-Salmon-Listings/ Salmon-Populations/Steelhead/Index.cfm), is in decline as shown by population census (1977–1990 average N=86.2, 1991–2004 average N=47.7, Ardren and Kapuscinski 2003; Johnson and Cooper 1992) and our estimates of LRS (Table 1). In spite of producing nearly twice the number of spawning adult offspring of OTS, even female RPS were not replacing themselves and their mates. Although repeatspawning fish have more breeding adult offspring per capita, because of low survival between breeding seasons, they contribute only ∼22% to the population output in terms of total numbers of offspring (Table 1). Survival from first to the second spawning season for female Snow Creek steelhead was ∼0.12. Given that female RPS produced more than 1.5 times the number of adult offspring as female OTS, survival to breed twice would have to increase to 0.35 for RPS to produce the same number of offspring as OTS. At current

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levels of smolt-to-adult survival, even if all females survived to spawn twice, the population would still not maintain itself. Assuming the relationship between the LRS of OTS and RPS stayed the same and at current levels of survival between spawning seasons, smolt-to-adult survival would have to double before the population became viable. If smolt-to-adult survival and survival between breeding seasons remains at current levels, the reproductive success of female RPS steelhead would have to increase from current levels by a factor of 4.0 for RPS females to produce the same number of offspring as OTS females and by a factor of 6.1 (reproductive success of RPS=11.3×reproductive success of OTS) for the population to become viable. Thus, programs that seek to recondition and then release post-breeding adults as a way to make a population viable (e.g., Gephard and McMenemy 2004) will not work unless steps are taken to address other aspects of survival. Acknowledgements We gratefully acknowledge the help of Thom Johnson, Randy Cooper, Cheri Scalf, and John Sneva (Washington Department of Fish and Wildlife) in procuring samples, providing data, and analyzing scales, and of Paul Bentzen for his thoughtful guidance. Financial support for this project was provided by the National Science Foundation (DEB-9903914) and the H. Mason Keeler Endowment (School of Aquatic and Fishery Sciences, University of Washington). The authors declare that they have no conflict of interest. This research was done in compliance with current University of Washington, Washington State and United States laws and regulations.

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