Sperm Competition in Salmon Hatcheries: The Need to Institutionalize Genetically Benign Spawning Protocols

Abstract

Salmon hatcheries in the Pacific Northwest historically spawned adults by combining eggs from several females and milt from several males in a single container. This mixed-milt approach leads to significant sperm competition and highly unequal genetic contributions from male spawners. Sperm competition substantially reduces the genetic effective number of breeders (N_b ) relative to the actual number of spawners (N_s ). Sperm competition in vitro can also result in undesirable artificial selection for life history traits (e.g., age or size at maturity) that are correlated phenotypically with sperm potency and fertilization success. A large number of salmon hatcheries in the Pacific Northwest, particularly those within some state agencies, continue to use mixed-milt fertilization despite documented genetic effects and potential risks. The continued use of mixed-milt fertilization may be due, in part, to insufficient genetic oversight of hatchery operations. As a general rule, salmon hatcheries should discontinue mixed-milt fertilization and institutionalize alternative spawning protocols that preclude or minimize sperm competition in vitro. Three alternative protocols are described here: pairwise spawning, nested spawning, and factorial or matrix spawning. The underlying premise of these alternative protocols is that every adult selected for use as broodstock should have an equal opportunity—and an equal probability—of producing progeny. A goal of most hatchery programs should be to minimize genetic change between the pool of returning adults available for broodstock each year and the progeny of parents selected as broodstock from that pool. To achieve this goal, spawning protocols should maximize N_b and minimize artificial selection associated with hatchery propagation. Such goals may require increased genetic oversight of hatchery operations comparable to the level of fish health oversight (pathogen monitoring and disease prevention) currently practiced in salmon hatcheries throughout the Pacific Northwest.

Notes

¹ Sperm potency refers to the fertilizing ability and success of sperm from a particular male, either as a function of the characteristics of the sperm itself (e.g. percent motility, longevity, etc.) or in direct competition with the sperm from other males during mixed-milt fertilization.

² The genetic effective number of breeders per year (N_b ) is the single-year equivalent of the genetic effective population size per generation (N_e ) for species in which multiple brood years, or age-classes constitute a single generation (Waples 1990, 2002a). In general, N_e ≈ N̄_b · g, where N̄_b is the arithmetic mean of N_b and g is the generation time in years or the mean age of spawners at reproduction such that males and females are weighted equally, that is, g = 0.5g_m + 0.5g_f , where g_m and g_f are the mean ages at reproduction for males and females, respectively.

³ An ideal population is defined as a population with an equal sex ratio, an equal and random probability of progeny survival to adulthood among parents, and a constant population size over time.

⁴ Responses (R) to natural or artificial selection in a population for a particular trait are measured by R = μ _P ′ − μ _P , where μ _P ′ and μ _P are the mean values of the trait in the progeny and the parental generations, respectively. The value of R can be predicted by R̂ = (V_a / V_P )(μ _S − μ _P ), where V_a is the additive genetic variance of the trait in the population, V_P is the phenotypic variance of the trait, and μ _S is the mean value of the trait among the selected parents (spawners). The μ _S value for each parent is weighted by the number of adult progeny produced by that parent. The quantity V_a /V_P is the heritability (h ²) of the trait (0 < h ² < 1.0), and μ _S − μ _P is the selection differential (R̂ = h ² · SD).

⁵ The relation N_e ≈ N̄_b · g does not apply to pink salmon because of their strict 2-year life cycle (g = 2) in which fish representing consecutive brood years (even and odd years) do not interbreed but instead represent two discrete populations. The entire population representing each year-class (even or odd) of pink salmon spawns within a single year, every other year. Thus, for pink salmon, N_e equals N_b.