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.

Keywords: age at maturity; conservation; delta smelt; domestication selection; heritability; phenotypic plasticity; relaxed selection.

FIGURE 1

Change in (a) age at maturity, (b) phenotypic variance, and (c) heritability over time for all fish in the hatchery in 2010–2021 (excluding 2011). Dotted black line in panel (a) indicates 52 weeks (the number of weeks in 1 year) for reference. Panels (b) and (c) show point estimates with 95% confidence intervals generated by the top model in Table S2.

FIGURE 2

Age at maturity relative to domestication index (DI) for regular season fish (i.e., excluding late season fish that experienced a different temperature regime) in 2010–2021 (excluding 2011). Panel (a) shows a linear regression of age at maturity and DI, with all years combined. Panel (b) shows the median age at maturity for four DI groups over time, with sample sizes for median calculations in Table S4. The dotted black line in both panels indicates 52 weeks (the number of weeks in 1 year) for reference.

FIGURE 3

Age at maturity relative to Julian birthday (a). Data are combined across the years 2010–2021 (excluding 2011) for regular season fish (i.e., excluding late season fish that experienced a different temperature regime), and regression lines are shown for each DI group. Dotted black line indicates 52 weeks (the number of weeks in 1 year) for reference. Panel (b) shows the mean age at maturity for each DI group, with error bars representing standard deviation.

FIGURE 4

Density of females that became ripe in the hatchery each week of the spawning season, in each year 2010–2021 (excluding 2011).

FIGURE 5

The mean number of offspring surviving to maturity (a measure of reproductive success) for parents in each DI group (a). We related the number of surviving offspring to each parent's (b) age at maturity and (c) week they were tagged as sexually mature, accounting for DI group in each analysis. Data are combined across the years 2010–2021 (excluding 2011) for regular season fish (i.e., excluding late season fish that experienced a different temperature regime), and regression lines are shown for each DI group.