Loss of plasticity in maturation timing after ten years of captive spawning in a delta smelt conservation hatchery

Abstract Adaptation to captivity in spawning programs can lead to unintentional consequences, such as domestication that results in reduced fitness in the wild. The timing of sexual maturation has been shown to be a trait under domestication selection in fish hatcheries, which affects a fish's access to mating opportunities and aligning their offspring's development with favorable environmental conditions. Earlier maturing fish may be favored in hatchery settings where managers provide artificially optimal growing conditions, but early maturation may reduce fitness in the wild if, for example, there is a mismatch between timing of reproduction and availability of resources that support recruitment. We investigated patterns of maturation timing in a delta smelt (Hypomesus transpacificus) conservation hatchery by quantifying changes to the median age at maturity since the captive spawning program was initiated in 2008. Over the span of a decade, we observed a small, but significant increase in age at maturity among broodstock by 2.2 weeks. This trait had low heritability and was largely controlled by phenotypic plasticity that was dependent on the time of year fish were born. Fish that were born later in the year matured faster, potentially a carryover from selection favoring synchronous spawning in the wild. However, higher DI (domestication index) fish showed a loss of plasticity, we argue, as a result of hatchery practices that breed individuals past peak periods of female ripeness. Our findings suggest that the hatchery setting has relaxed selection pressures for fish to mature quickly at the end of the year and, consequently, has led to a loss of plasticity in age at maturity. Hatchery fish that are re‐introduced in the wild may not be able to align maturation with population peaks if their maturation rates are too slow with reduced plasticity, potentially resulting in lower fitness.

Supplementary material for "Loss of plasticity in maturation timing after ten years of captive spawning in a delta smelt conservation hatchery" Table S1: For each spawn year, the median, standard deviation, and sample size for age at maturity (number of weeks from fertilization to the expression of gametes).

Year
Median  Eggs are incubated at 16.5˚C and juvenile are reared at this temperature until late fall when the temperature is lowered to 12˚C to reduce stress from handling during tank transfers.Regular season fish (orange) are kept at 12˚C until spawning, while late season fish (green) have temperature increased back to 16.5˚C after handling for as long as possible before lowering back to 12˚C for spawning.Both groups experience the higher temperature (16.5˚C) for approximately the same total length of time, however the regular season fish experience the higher temperature for one continuous time period, while the late season fish experience the higher temperature in a discontinuous manner.

Figure S1 :
Figure S1:Temperature regimes experienced by regular season fish (orange) and late season fish (green) over the course of their ~1 year life span.Eggs are incubated at 16.5˚C and juvenile are reared at this temperature until late fall when the temperature is lowered to 12˚C to reduce stress from handling during tank transfers.Regular season fish (orange) are kept at 12˚C until spawning, while late season fish (green) have temperature increased back to 16.5˚C after handling for as long as possible before lowering back to 12˚C for spawning.Both groups experience the higher temperature (16.5˚C) for approximately the same total length of time, however the regular season fish experience the higher temperature for one continuous time period, while the late season fish experience the higher temperature in a discontinuous manner.

Figure S2 :
Figure S2: Range of dates fish were tagged as sexually mature during each spawning season in 2010-2021.

Figure S3 :
Figure S3: Age at maturity by year for fish maturing in 2010-2021, separated by temperature regime (regular season versus late season; see Figure S1).Points are jittered within year to increase visibility.Each line represents the linear regression for the color-coordinated temperature regime.

Standard deviation Sample size
Models with random effects were evaluated with DIC (Deviance Information Criterion) values for fish maturing in years 2010 and 2020.The models with lowest DIC were selected for inclusion of random effects.Models with corresponding fixed effects were evaluated with posterior distributions (PD).Effects that with 95% confidence intervals overlapping zero were not included in the final model.AgeAtMaturity = number of days until male or female fish ♱2010 was not a good representation for testing the inclusion of DI fixed effects because only low DI fish were present in 2010.

Table S3 :
All variance components (in weeks) for offspring age estimated from animal models (age at maturity in 2010 to 2021).N: number of offspring in animal model.VA: additive genetic variance.VP: Total phenotypic variance.VDamID: Variation due to dam identity.In parentheses are 95% confidence intervals.All variance components are reported as modes from 1800 iterations of the model.

Table S4 :
Sample sizes for calculating median age at maturity for each DI group in each spawn year, using only regular season fish.