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).