4.4 | Fluctuating selection and maintenance of adaptive diversity
Our results suggest the presence of a temporal portfolio effect, where a multi-age population with overlapping generations maintains a portfolio of genotypes (Ellner and Hairston 1994). The interannual variation in oceanic conditions and its effects on the selection of POP during their first year at sea prior to settlement may be thought of as a “Selective Sieve” (Figure 5), where each year presents different sets of selection pressures during the early developmental life stage. The selection pressures, in the form of various environmental drivers such as ocean temperatures, productivity (chlorophyll-a) and their timing vary from year to year resulting in some phenotypes being detrimental in one year, but advantageous in another when encountering highly diverse pelagic habitats. The selective sieve is therefore specific to the year of the POP pelagic life stage, and therefore unique to each cohort which then contains alleles favored by the conditions of their first year. In these long-lived species with lifespans of over 100 years, in any one year the larval cohort at parturition may be the result of breeding across dozens of spawning aged cohorts (~ 8 to 100 years old or more). The parental cohorts contain many alleles that are representative of the selection due to oceanic conditions during their first year at sea. At parturition, the POP larvae contain all of these alleles, however, from parturition to settlement, some of the alleles prove to be deleterious as the oceanic conditions do not favor them, and only a subset of the larvae containing the advantageous alleles survive until settlement. This is an example of fluctuating selection (Bell 2010; Kawecki 2000; Lande 2007), where the direction of selection is constantly changing between generations. The species’ life history of long reproductive period relative to the time-scale of fluctuating selection maintains genetic diversity that is adaptive across a range of environmental variation.
Population viability in fish employing broadcast spawning strategies is especially vulnerable to changing oceanographic conditions. Ocean currents may advect YOY far offshore where they will fail to reach their shelf-slope nursery areas. Using ROMS-based models, Stockhausen et al. (2018) showed that up to 70% of the YOY failed to reach suitable nursery habitats prior to wintertime and were not expected to survive. The ones that are not advected out of reach of nursery habitat must still acquire sufficient lipid reserves in order to settle out and overwinter. Interannual differences in ocean temperatures, prey and predator abundances and composition will also affect whether the YOY will survive to reach their nursery habitats with sufficient lipid reserves to overwinter and eventually recruit to the population. Maintaining a high diversity in phenotypes through cohort-specific selection may be thought of as a form of diversification bet hedging response to a fluctuating natural selection as described by Simons (2009).
These results underscore the importance of maintaining many cohorts in order to maximize the population resilience to environmental variability. POP are vulnerable to age truncation where older fish are more likely to be fished since they are exposed to fishing longer (Berkeley 2004). The importance of maintaining older age classes in marine fishes has long been recognized as being a factor in their recruitment (Longhurst, 2002; Hixon et al., 2013). Hanselman et al. (2005) noted that age truncation has occurred in POP due to unrestricted fishing in the past which led to disproportional absence of 40+ year old fish. However, the mechanism of adaptation through maintenance of age-specific advantageous alleles would be compromised if whole cohorts are inadvertently fished by depriving populations of the advantageous alleles specific to that cohort.
The uniqueness of the demonstrated cohort-specific selection signatures may allow for reconstruction of past oceanographic conditions based on the alleles present in a given cohort. The 2015 cohort will therefore represent the alleles favored (or conversely lost) during especially warm oceanic conditions as experienced during 2015. It may be possible that by examining allele frequencies in an adult cohort, of for example 50-year-old fish, the selection pressures encountered during their YOY stage may be revealed. Furthermore, ageing of adults based on cohort-specific allelic signatures may also be possible by maintaining cohort-specific selected allelic signatures. This may prove especially useful since otolith ageing of POP adults is fairly error prone especially for older fish (>20 years old) (Beamish, 1979; Stanley, 1986).