Figure 4.
Relationships between pup
emergence date and fitness proxies. Panel a presents the output of our
selection model examining the relationship between pup emergence date
and the weighted proportion of pups surviving their first winter. Panel
b presents the output of our selection model examining the association
of pup emergence date with the total number of pups surviving their
first winter. The black line represents the prediction from the models.
The grey shading is the associated confidence intervals. Data points
have been jittered to enable clearer visualization (number of females =
176; number of litters = 417).
Discussion:
We found that pup emergence date was weakly linked to female emergence
date, with late emerging females mating in their burrow and early
emerging females delaying reproduction. We found a positive effect of
spring snowpack on the timing of pup emergence, but no effect of spring
temperature. We found directional, but not stabilizing selection for pup
emergence date, with pups that emerged earlier better surviving their
first winter. We additionally found among-individual variation at the
female level in pup emergence date, but no additive genetic basis for
that variation. While there was population-level plasticity in response
to average spring snowpack, there was no inter-individual variation in
plasticity for either average spring snowpack or temperature.
We showed a weaker relationship between female and pup emergence date
than expected. Indeed, there was substantial variation in pup emergence
date, with the earliest pup emerging about a month before and the latest
emerging about a month later than expected based on their mother’s
emergence date (Figure 1). Gestation and lactation length were assumed
to have a fixed duration (30 and 25 days respectively), but there might
be some among-individual variation in both of their lengths.
Yellow-bellied marmots are considered capital breeders and mate when
little to no food is available in the environment (Armitage, 2014).
Therefore, the body condition of a female might shorten or lengthen
gestation by a few days. During lactation, most females have emerged
from their burrow and thus both a female’s body condition and
micro-environmental variation in food availability could lead to
inter-individual variation in lactation length before pups are weaned.
Again, variation by a few days is expected. Overall, among-individual
and environmental variation in gestation and lactation length, would
only explain a variation by a few days in the relationship between pup
emergence date and their mother’s emergence date. Given that pups could
emerge up to a month before and up to a month after expected based on
their mother’s emergence date, it is clear the females are in some cases
delaying reproduction after emerging and in others, able to mate in
their burrow before emerging. Females delaying reproduction after
emerging might be due to environmental variation, poor body conditions,
and/or the absence of a male to mate with. Indeed, our results showed
that pup emergence date was related to spring snowpack, with pups
emerging later in springs with heavier snow (Table 2). This possibility
of delaying reproduction because of spring snowpack may also explain why
pup and adult emergence date are not similarly associated with spring
temperature. Given that the date of emergence from hibernation of adult
marmots is strongly related to spring temperature, (Inoyue et
al. , 2000; Edic et al., 2020), we would also expect a positive
relationship between pup emergence and spring temperatures. Yet, we find
no association of spring temperature with pup emergence date (Table 2)
and therefore, female marmots may delay their reproduction until there
is less snow regardless of spring temperatures.
However, Andersen et al. (1976) postulated that delaying
reproduction decreased fitness as the growing season was shortened for
pups and females. Indeed, we found directional selection for earlier pup
emergence even though females are emerging earlier from their
hibernacula (Edic et al., 2020) and growing season length has
increased (Cordes et al., 2020). To elaborate, litters that
emerged earlier had increased probability to survive and increased
number of pups surviving to one year old than litters that emerged
later, indicative of directional selection (Table 4). This may be a
result of increased time during the growing season to forage and gain
weight when pups are born earlier in the season (Monclús et al. ,
2014). Further, earlier born pups tend to be heavier at weaning than
later born pups and this weight is positively correlated with overwinter
survival (Monclús et al. , 2014). We do not find a similar pattern
with litter size (Table 4). Given the selective pressures for earlier
births in the marmots, we would predict that females that reproduce
later in the season would produce fewer, but heavier pups than those
females that reproduce earlier (Stearns, 1992). Indeed, it is predicted
that in unfavourable environments, it is advantageous to not reproduce
to your full capacity (Monclús et al. , 2011). However, in our
study, it seems that regardless of the fitness costs associated with
giving birth later in the season, females will give birth to the same
number of pups regardless of when they will emerge. This may stem from
previous stabilizing selection on the number of pups that can be
produced. Further, Monclús et al. , (2014) report that mothers
will not attempt to provide the offspring born later with more resources
compared to offspring born earlier to mitigate the effect of being born
later. Therefore, even though pups born later in the season will have
lower survival, mothers will not invest more resources in them to reduce
the fitness costs (Monclús et al. , 2014).
Despite these existing directional selection pressures to reproduce
early, pup emergence date will not show an evolutionary response because
of its low additive genetic variation (Table 3). There are two plausible
explanations for this low variation. First, female marmots can re-absorb
fetuses if they are not viable. By using pup emergence date as a proxy
for the timing of reproduction, we are effectively removing all those
females that may have reproduced, but not given birth to any pups. This
removes a potentially significant source of variation in the trait and
may explain the lack of observable heritability. If females reproducing
too early or late tend to reabsorb or abort their pregnancies, this may
also decrease variation through stabilizing selection. Secondly, the
timing of reproduction is a fitness trait and fitness traits are
generally reported to be less heritable compared to other traits (Merilä
& Sheldon, 2000). This phenomenon is generally attributed to Fisher’s
fundamental theorem (Price & Schluter, 1991) which proposes that there
should be strong selection on fitness traits that maximally increase
fitness (Merilä & Sheldon, 2000). This reduces the heritability by
reducing the amount of variation in the trait – only the variation that
provides the greatest fitness benefit will be left in the population
following this strong selection (Merilä & Sheldon, 2000). This may
explain the pattern we observe here. There may have been strong
selection on the timing of pup emergence date to increase fitness,
causing a reduction in the amount of additive genetic variance present
and as a result lowering the heritability of the trait. However, there
have been challenges to this theorem with suggestions that the lower
heritability of fitness traits is not due to decreased additive genetic
variance, but rather increased residual (Merilä & Sheldon, 2000), or
environmental variance (Price & Schluter, 1991). In our model we report
both low additive genetic variance and high residual variance.
Past selective pressures may also explain why we found no
inter-individual variation in the plasticity of pup emergence date with
spring snowpack (Figure 3). Female marmots are responding in the same
way to the same changes in average spring snowpack. Inter-individual
differences in the intercept in our plasticity model indicated that in
the average environment, individuals are reproducing at different times
(Nussey et al. , 2007). No covariation between the intercept and
the slope indicated that there is no relationship between the timing of
reproduction in the average environment and how plastic an individual is
(Brommer, 2013). The lack of inter-individual variation in the slope in
our population indicated that individuals do not differ in their
response to changes in the environment. This may be explained by
canalization (Stearns, 1982). Marmots are heavily constrained by their
climate and have a relatively short period of time to reproduce and gain
mass again prior to hibernating. Since there is strong selection to
reproduce within a short window of time where fitness is optimized, and
strong selection is expected to decrease the magnitude of
inter-individual differences (Westneat et al. , 2009), this may
explain the lack of IxE in our study population. Predation might also
drive the small variation. If females varied substantially in the timing
of their reproduction in response to the same environmental conditions,
pups would emerge at different times, exposing them to increased
predation risk as there are fewer pups available at any given time as
prey (Michel et al., 2020).
Significant sources of variation in our animal model were valley,
permanent environment, and year (Table 2; Table 3). Pup emergence date
is earlier in the down-valley compared to the up-valley. This is to be
expected as these two sites differ in elevation by about 200 m, causing
a two-week delay in the phenology of the up-valley compared to the
down-valley (Monclús et al. , 2014). Inter-individual variation in
pup emergence date may be due to microenvironmental differences
experienced by females such as burrow quality, foraging ability, or
differences in environmental conditions experienced (e.g., trees
preventing snow melt; van Vuren & Armitage, 1991). Inter-annual
variation in pup emergence date may be expected due to yearly variations
in environmental conditions such as variation in the number of males
present or amount of snow in the area. We find no association of colony
area with the date of pup emergence, but this may be because permanent
environment effect and colony are correlated as females do not generally
leave once they are reproductively mature (Edic et al., 2020).
Colony effects that may have been confounded with permanent environment
may be the number of individuals present, as marmots can produce more
pups when there are fewer individuals in the colony (Maldonado-Chapparroet al., 2015), the number of males present in the colony, or the
degree of reproductive suppression present in the colony. These factors
could all impact the timing of reproduction in a colony-specific way.
For the model examining the annual number of pups surviving their first
winter, we found that more pups survive their first winter in the
up-valley compared to the down-valley (Table 4). This is likely due to
differing predation rates between the valleys, with higher predation in
the down-valley compared to the up-valley. Predation and winter
conditions are the main causes of death in marmots, and young marmots
are very susceptible to predation (Armitage, 2014). For the models on
litter size and annual number of pups surviving, we report a positive
effect of a mother’s mass in June (Table 4). June body mass of a mother
has been reported to have a positive effect on the mass of her
offspring, and heavier offspring are expected to have higher chances of
overwinter survival (Monclús et al. , 2014). Additionally, as
marmots are capital breeders, higher body masses are often associated
with more resources available for reproduction, potentially explaining
larger litter sizes for larger females.
There are some limitations to our dataset that may have impacted our
results. First, despite best efforts, we might have some error on
emergence date for pups and mothers because we rely on visual
observations to determine emergence. While our observation effort is
high in this study with colonies observed on a near-daily basis with
approximately 1000 hours of observations logged per year, exact
emergence dates may still be missed. We additionally tried to control
for this by limiting our analyses to only the main colonies as these are
observed with a higher frequency than satellite colonies. Therefore, we
are less likely to have missed emergence dates in the main colonies
compared to the satellite colonies. Further, we are only able to use pup
emergence date as our proxy for the timing of reproduction. Being able
to see inside burrows and know exactly when pups are born would provide
a better estimate of the timing of reproduction in addition to
identifying cases when all pups died during lactation. Similarly, being
able to know when a female mated would also provide more information
about pregnancy interruption (reabsorption and abortions). Additionally,
we unfortunately only have data on female emergence date between
2003-2017. It would have been interesting to analyze pup and female
emergence dates for more years. Finally, since we only have one weather
station on site, the climate variables used are the same between
valleys. In the future it would be interesting to separate weather
variables between the valleys since the up-valley environment is harsher
and there is phenology delay of about two weeks between the valleys.
Conclusions:
Overall, we report that while marmots are plastically adjusting the
timing of pup emergence date in response to changing spring snowpack,
individuals do not differ in their plasticity level. Further, pup
emergence date is not heritable but there is selection for pups to
emerge earlier. This indicates that pup emergence date may not have an
optimum time and it is just better to emerge earlier. Without having
inter-individual variation in plasticity and without being able to
evolve in response to natural selection, this population may be limited
in its ability to track optimal environmental conditions for
reproduction. If climate continues to change, this may prove
problematic. For instance, the length of the active season may change,
altering the timing of food availability. If pups do not emerge early
enough, they may not be able to gain enough mass prior to hibernation.
Similarly, if the mother reproduces too late in the season, she will
also be limited in her ability to gain sufficient mass for hibernation.
This potential mismatch in the length of the active season and when pups
emerge may impact population fitness, causing a decrease in pup and dam
survival. Additionally, future research should investigate the
discrepancy we report between female and pup emergence to determine the
ecology behind this pattern.