Introduction
Phenotypic plasticity allows organisms to thrive in environments that
are variable in space and time (Stearns, 1989). A key source of
environmental variability is the seasonal cycle, which brings changes in
temperature, weather, food availability and predation rates across the
year. While often dramatic, seasonal changes can be predicted and
anticipated through environmental signals, such as changes in the length
of day versus night (Bradshaw & Holzapfel, 2007). Therefore, an
organism may achieve high fitness at different times of year through
seasonal plasticity: the controlled expression of seasonally appropriate
body forms, physiologies, or behaviors (Shapiro, 1976; Moran, 1992;
Varpe, 2017).
Plastic responses sometimes include suites of traits working together to
form complex alternative strategies, as is seen with predator defense
morphs in juvenile frogs (McCollum & Van Buskirk, 1996), paedomorphic
versus metamorphic development in salamanders (Semlitsch et al., 1990),
migratory polyphenism in locusts (Pener & Simpson, 2009), and indeed
with environmentally controlled sex differentiation in many organisms
(Ah-King & Nylin, 2010). Such examples suggest that in the presence of
an adaptive plastic response on one trait axis, selection can be
expected to favor co-adaptive fine-tuning on additional trait axes.
In the case of seasonal plasticity, many insects and other arthropods
have the facultative ability to either enter diapause (a hormonally
controlled resting state) at a given life stage, hence postponing
reproduction until the following year, or develop directly to adulthood
and attempt to reproduce (Tauber et al., 1986). Besides the various
physiological changes inherent to diapause itself (increased stress
tolerance; etc.), a decision to diapause or not also determines the
amount of time stress placed on an individual relative to the end of the
favorable season, which in turn predicts changes in the optimal values
of core life history traits such as growth rate and body size (Abrams et
al., 1996). In other words, an individual destined for diapause can
afford to develop slowly, while averting diapause and attempting to fit
an additional reproductive cycle into the same year may necessitate
faster development, implying rapid growth and/or a smaller adult size.
Diapausing and nondiapausing individuals will also experience different
temporal environments as adults, which enables divergent selective
pressures on adult size and morphology (Van Dyck & Wiklund, 2002).
Correlations between diapause decision and life history traits,
especially development rate and body size, have been predicted through
optimality modelling (Kivelä et al., 2013) as well as empirically
observed (Nylin, 1992; Blanckenhorn & Fairbairn, 1995; Aalberg Haugen
et al., 2012; Friberg et al., 2012; Esperk et al., 2013; Aalberg Haugen
& Gotthard, 2015). However, little is still known about the ontogeny
and mechanistic details of these co-adapted diapause/nondiapause
phenotypes.
For an insect using seasonal cues to determine whether or not to enter
diapause, cues perceived later in life (or during a longer period of
time) should be more likely to accurately predict the future selective
environment, which suggests that it may be favorable to postpone the
diapause decision to gather more information. However, a potential
tradeoff lies in the fact that the later a decision is made, the smaller
the scope for differentially expressing any co-adapted traits that
diverge downstream of the diapause switch (Friberg et al., 2011). The
severity of this tradeoff may depend, in turn, on the extent to which
the set of traits constituting the diapause/nondiapause phenotypes are
regulated independently of one another. One extreme possibility is that,
once induced by seasonal cues, individuals are irreversibly channeled
into one of two distinct developmental programs, each with a
corresponding set of trait values (Nijhout, 2003). Alternatively, traits
may be induced independently of one another, but by the same
environmental cues as the diapause switch (Mather, 1955), or pathway
choice may be reversible by cues experienced later in development. While
these latter scenarios would allow for more time to develop optimal
trait values, they may also increase the risk of producing intermediate
phenotypes of low fitness, through developmental instability or
conflicting cues (Moran, 1992; DeWitt et al., 1998). Finally, there is
the possibility that the expression of one trait indirectly affects the
expression of another. In particular, plastic regulation of development
rate early in the insect’s life may determine which regulatory stimuli
it becomes exposed to later on, hence phenotypes are molded into two
overall responses under natural conditions (slow-growing diapausers
versus fast-growing non-diapausers). This scenario would correspond to
the “cascade”-style developmental switch described by West-Eberhard
(2003).
In a study of three butterfly species, each from a lineage that has
seemingly separately evolved diapause in the pupal stage, Friberget al. (2011) showed that the photoperiodic switch controlling
whether or not to enter diapause is “locked in” relatively late in
larval development. In other words, the daylength experienced last
determined diapause decision, to a large extent overriding earlier
experiences. However, for all three species, regulation was asymmetric:
a decision to enter diapause could be reversed later in life than could
a decision not to enter diapause, likely reflecting the relative amounts
of time required to adequately prepare for each respective pathway.
Further investigations in one of the species, Pieris napi ,
revealed that the diapause and non-diapause pathways differed in growth
rate after, but not before, the final decision had been made, indicating
that to a large extent pathway trait differences accumulate downstream
of the diapause switch (Friberg et al., 2012). Here, we build on these
previous results by examining the ontogeny of the diapause/nondiapause
polyphenism in another of the three butterfly species, Pararge
aegeria . By manipulating photoperiod regimes at different points during
the larval period, we investigate how early the two pathways diverge in
terms of development rate and body size. Furthermore, we test to what
extent growth decisions are reversible by changes in photoperiodic
information during development, and whether the strategic asymmetry seen
in the regulation of diapause decision is also reflected in the
regulation of these co-adapted life history traits.