Discussion
Phenotypic plasticity involves phenotypic changes associated with
environmental conditions, and may favor the establishment or persistence
of organisms in changing environments (Ghalambor et al. , 2007).
Consequently, plasticity may potentially affect the selective pressures
that a population encounters and, as a result, its evolutionary
trajectory (Oster & Alberch, 1982; Bonduriansky et al. , 2012).
Our experiment illustrates how within- and transgenerational plasticity
can ameliorate the impact of stressful thermal conditions on
physiological and fitness-related traits. In this context, our main
results can be summarized as follows. First-generation flies subjected
to a variable and, stressful thermal environment exhibited higherCTmax when compared against their counterparts
maintained at a constant temperature. This plastic and seemingly
adaptive response came at costs, however, since these flies also
exhibited lower survival rates, fecundity (Figure 3), and, ultimately,\(R_{0}\) and Tg (Figure 2). Interestingly, these
maladaptive plastic responses were less evident in their offspring
(Figures 2 and 3), suggesting partial compensation mediated to some
degree by transgenerational plasticity.
We aimed to compare the response of the flies under variable and
constant thermal environments using both direct measures of fitness and
physiological proxies of fitness, such as thermal tolerance, and results
were dramatically different (Figure 3). Contrary to results by
Nyamukondiwa et al. (Nyamukondiwa et al. , 2018) who evaluated the
influence of thermal variability on heat tolerance, our results show
that CTmax was positively affected by thermal
variability, although with adverse effects on fitness.
These results are intriguing because the temperature peak in the
variable thermal environment (32ºC) was substantially lower than the
estimated CTmax (~ 39ºC), and yet
this temperature was clearly stressful and impacted survival (Figure 3).
Although the impact of temperature peak and time of exposure to thermal
extremes on organisms cannot be disentangled, the differences in
exposure time might explain this counterintuitive result, since the
temperature range that organisms can tolerate is associated with the
duration of thermal stress (Rezende et al. , 2014). Consequently,
prolonged exposure to high and yet less extreme temperatures elicited an
increase in CTmax at a cost in survival and, more
importantly, in fecundity rates that are suggestive of a trade-off since
less energy could be allocated to reproduction. These results agree with
Folguera et al. , (2009) who reported that high environmental
thermal amplitude experienced by terrestrial isopods increased the
synthesis of stress-inducible heat-shock proteins (HSP), but at a
metabolic energy cost with negative effects on longevity and growth
rate. Not only is the production of HSP metabolically expensive (e.g.,
protein biosynthesis represent nearly 30-50% of total cellular energy
consumption(Krebs & Loeschcke, 1994; Krebs & Feder, 1997, 1998)), but
also they require ATP to maintain the structural integrity of other
proteins (Hochachka & Somero, 2002). In this sense, although plastic
responses may mitigate the adverse effects of thermal stress, their
compensatory effects might be limited by energetic trade-offs
(Pigliucci, 2001; Bozinovic et al. , 2016). Consequently, several
studies work with the assumption that higher heat tolerance is a
beneficial trait (Cavieres et al. , 2016; Sørensen et al. ,
2016; Salachan & Sørensen, 2017; Salinas et al. , 2019), but here
we show that this response was accompanied by a decrease in survival and
fecundity, highlighting the importance of incorporating direct measures
of fitness in physiological studies in order to have a broad
understanding of the implications of phenotypic changes in response to
environmental inputs.
Interestingly, fitness cost of living under a variable temperature
decreased significantly in the second generation, providing evidence of
partial compensation to a stressful thermal environment. This
cross-generational compensatory response involves a 133% increase inR0 in the F1 in comparison to P
(R0 = 259 in VV versus 111 eggs/female in V), but
values were still 25 % lower than in flies reared at a constant
temperature (R0 = 325 eggs/female). In this
context, our results agree with previous studies that have documented
that parental experience modifies the response to environmental input in
their offspring. For instance, rapid compensatory responses in tolerance
and/or reproductive output have been described in the marine polychaeteOphryotrocha labronica subjected to a low CO2environment (Rodríguez-Romero et al. , 2016) in Daphnia
magna (Gustafsson et al. , 2005) raised with toxic cyanobacteria
or coral reef fish Acanthochromis polycanthus (Donelson et
al. , 2016) exposed to high temperature (see also(Jensen et al. ,
2014; Thor & Dupont, 2015). Overall, these studies suggest that
populations can respond rapidly to pronounced environmental changes,
providing putative evidence that non-genetic inheritance might underlie
observed responses to rapid changes in climatic conditions (Rando &
Verstrepen, 2007).
The potential impact of selection should not be dismissed, however.
Recovery of reproductive output reported in the literature and in our
study might result from the synergistic effects of within-generation
plasticity and genetic adaptation(Rodríguez-Romero et al. , 2016).
As has been recently pointed out, estimates of transgenerational
plasticity can be biased due to selection and this is the case even in
half- or full-sibs designs(Santos et al. , 2019). Consequently,
these effects are particularly relevant in studies dealing with
responses to stressful environments employing outbred populations (e.g.,
this study or results for O. labronica (Rodríguez-Romero et
al. , 2016)), which is a problem often neglected in the literature of
transgenerational effects (Ho & Burggren, 2010; Burggren, 2014). For
instance, the drop in survival and fecundity in P flies from V may
impose strong selection and observed responses in F1 could partly
reflect adaptive responses in the Darwinian sense. While the growing
evidence indicates that natural populations can respond rapidly to
environmental changes, resulting in full or partial compensatory
responses to an environmental stress, caution is warranted regarding
inferences on the mechanistic basis underlying these responses (Santoset al. , 2019).
To summarize, here we describe how an outbred population of D.
melanogaster responds rapidly changing thermal conditions within and
across generations. Our analyses provide evidence of a trade-off between
thermal tolerance and fitness components such as fecundity in parental
flies and pronounced albeit incomplete compensatory responses in their
offspring. Similar approaches are necessary to extend studies from
within- generational responses to responses across multiple generations.
In this context, we urge future research to be tailored to specific
climatic scenarios or geographic regions, aiming to build explanations
and predict, in the near future, the potential responses of natural
populations to ongoing global warming.