Keywords (6-10)
Reproduction, phenotypic plasticity, microevolution, climate change,
quantitative genetics, Marmota flaviventer
Abstract:
With global climates changing rapidly, animals must adapt to new
environmental conditions with altered weather and phenology. Key to
adapting to these new conditions is adjusting the timing of reproduction
to maximize fitness. Using a long-term dataset on a wild population of
yellow-bellied marmots (Marmota flaviventer ) at the Rocky
Mountain Biological Laboratory (RMBL), we investigated how the timing of
reproduction changed with changing spring conditions over the past 50
years. Marmots are hibernators with a four-month active season. It is
thus crucial to reproduce early enough in the season to have time to
prepare for hibernation, but not too early so as snow cover prevents
access to food. Importantly, climate change in this area has increased
spring temperatures by 5 oC and decreased spring
snowpack by 50 cm over the past 50 years. We evaluated how female
marmots adjust the timing of their reproduction in response to the
changing conditions and estimated the importance of both genetic
variance and plasticity in the variation in this timing. We showed that,
within a year, the timing of reproduction is not as tightly linked to
the date a female emerges from hibernation as previously thought. We
reported a positive effect of spring snowpack but not of spring
temperature on the timing of reproduction. We found inter-individual
variation in the timing of reproduction, including low heritability, but
not in its response to changing spring conditions. There was directional
selection for earlier pup emergence date since it increased the number
and proportion of pups surviving their first winter. Taken together, the
timing of marmot reproduction might evolve via natural selection,
however, plastic changes will also be extremely important as long as
plasticity is not limited. Further, future studies on the marmots should
not operate under the assumption that females reproduce immediately
following their
emergence.
Introduction :
Life history traits are those that impact the fitness of an individual
through survival and/or reproduction (Braendle et al., 2011). The
seasonal timing of these traits is heavily dependent on environmental
conditions (Brommer, 2000; Bronson, 2009). These environmental
conditions can vary inter-annually (Bright Ross et al., 2020) and
seasonally, in both the mean value of the environment and in the timing
of important events (e.g., when food becomes available; Nusseyet al., 2005). Animals must react to these yearly and seasonal
variations by adjusting the timing of their life history traits to
coincide with the environmental conditions that will maximize survival
and/or reproduction. For example, timing egg laying date so that
offspring emerge when food availability is at its highest (Nusseyet al., 2005), timing changes in coat colouration to match
seasonal changes in the environment and thus avoid predation (Millset al., 2013), and timing emergence from hibernation to emerge
late enough that food resources are not covered by snow, but early
enough to maximize the length of the active season (Edic et al.,2020). However, climate change may directionally shift when these
environmental conditions occur (Mills et al., 2013; Nusseyet al., 2005). Indeed, this has been seen with shifts in the
timing of food availability (Nussey et al., 2005) and changes in
average season lengths (Cordes et al., 2020). These changes can
lead to mismatched timing between animal behaviours and optimal
environmental conditions if animals are not able to adjust their timing
adequately. Consequently, fitness can be negatively impacted, and indeed
declines in both reproductive success (Nussey et al., 2005) and
survival (Cordes et al., 2020) have been reported.
Animals can alter the timing of their life history traits to coincide
with the changed timing of environmental conditions through phenotypic
plasticity and/or microevolution (Boutin & Lane, 2014).
Phenotypic plasticity occurs when a phenotype changes in response to a
changing environmental condition (Nussey et al., 2007). This can
be measured in a wild population by observing how a trait that is
expressed multiple times during an individual’s life changes in response
to changes in climate (Nussey et al., 2007). Phenotypic
plasticity is an important mechanism by which individuals respond to
their environment as it allows for a fast change in the phenotype that
can accurately track sudden changes in environmental conditions
(Charmantier et al., 2008). Plasticity therefore also provides a
potentially important solution in terms of climate change response
because while the trend in climatic changes is expected to be
directional (Boutin & Lane, 2014), variability is expected to increase
(Childs et al. , 2010). Indeed, Charmantier et al. (2008)
outlined how the egg-laying date of a population of great tits
(Parus major ) in the UK has become earlier by 14 days. They
attributed this finding to phenotypic plasticity in response to changing
spring temperatures with microevolution playing no role. While there is
population-level plasticity, they reported no inter-individual variation
in plasticity amongst females. This lack of variation indicated that
there is no individual by environment interaction (IxE; Nussey et
al., 2007) for the date of egg-laying in this population.
However, the capacity of phenotypic plasticity to respond to these
global environmental changes may be limited over the long-term (Boutin
& Lane, 2014). Certain studies have shown that to fully adapt to
changes in climatic conditions, populations will need to undergo
microevolutionary changes as phenotypic plasticity will not be enough on
its own (Phillimore et al. , 2010; Mills et al., 2013). For
instance, Phillimore et al. (2010) examined the response of first
spawning date in British populations of the common frog (Rana
temporaria ) to changes in temperature. They found that even though
spawning date is plastic, plasticity alone will not be enough to adapt
to the degree of change in temperature expected in these areas. They
outlined that the upper limit of plasticity in this population is a
5–9-day advancement in spawning date. However, to maintain fitness,
these populations will need to spawn 21-39 days earlier. Therefore,
microevolutionary changes will be needed to allow the population to
fully adapt. Further, the timing at which certain animals molt to match
their environment has become mismatched with current environmental
conditions (Mills et al., 2013). In these systems, spring snow
melt now begins before coat colouration has changed, leaving individuals
vulnerable to predation (Mills et al., 2013). Mills et al.(2013) studied wild populations of snowshoe hares (Lepus
americanus ) and determined that while there was plasticity in the rate
of molting in the spring, it is not enough to cope with the magnitude of
expected climate change. Indeed, they reported that with current climate
change projections, in the next hundred years hares will be exposed four
to eight times longer than presently unless microevolutionary changes
occur in the timing of spring molt.
These microevolutionary changes can occur in plasticity or in the mean
of the trait if there is inter-individual variation, heritability, and
selection. In terms of microevolution in plasticity, Nussey et
al. (2005) found increased selection pressures for higher plasticity in
the egg-laying date in a population of great tits (Parus major )
in response to warming temperatures. They concluded that selection for
increased plasticity is being observed because those individuals that
can adjust the timing of their egg-laying date to better match
environmental conditions (i.e., those that have increased
plasticity), will have more food available for their young when they
hatch. This would increase offspring survival compared to those
individuals with lower plasticity. They also found that plasticity is
heritable and there is inter-individual variation in the degree of
plasticity expressed. In terms of microevolution on the mean of the
trait, Réale et al. (2003) reported that over the course of a
decade, the date of reproduction in a wild population of red squirrels
(Tamiasciurus hudsonicus ) became 18 days earlier. By finding that
this trait is heritable and under strong negative selection, they
concluded that this change in birth date is due, in part, to
microevolutionary changes in the mean of the trait (but see Boutin &
Lane, 2014). However, while microevolution may offer a long-term
solution in responding to climate change, there may be a mismatch
between the two (Gienapp et al., 2007; Boutin & Lane, 2014).
Microevolution is a relatively slow, and not easily adjustable process
in contrast to phenotypic plasticity; this may prove problematic as a
response to climate change which can occur quickly and vary
inter-annually (Charmantier et al., 2008).
Despite the extensive background research on these topics, studies
examining the relative contributions of phenotypic plasticity and/or
microevolution in the response of a wild population to climate change,
remain rare (de Villemereuil et al. , 2020; Nussey et al. ,
2005; Lane et al., 2018). This is because studies of this nature
require long-term data, a known pedigree, a sizeable population (Boutin
& Lane, 2014; Nussey et al., 2005), and a study site that is
impacted by climate change (Lane et al., 2018). One example of a
study system that meets these requirements are the yellow-bellied
marmots (Marmota flaviventer ) of the Rocky Mountain Biological
Laboratory (RMBL) in Colorado, USA. Since 1962, this study system has
generated annual data on individual marmots, maternity has been assigned
behaviourally since the study’s beginning and paternity assignment began
in 2000. For the past 50 years, there has been a steady increase in mean
temperatures and decrease in mean snowpack, with one of the fastest
reported changes globally. Specifically, there has been an increase of 5oC in average spring temperatures and a decrease of 50
cm in average spring snowpack over the past 50 years (Figure S1).
Coupled with these climatic changes are changes in the marmots’ life
history: adult emergence date from hibernation has advanced (Edicet al., 2020), pups are being weaned earlier (Ozgul et
al., 2010), and overwinter survival is decreasing while summer survival
is increasing (Cordes et al., 2020). Indeed, a marmot’s life
history is heavily constrained by climate (Cordes et al., 2020).
During the short four-month growing season, marmots must gain as much
weight as possible to survive hibernation (Ozgul et al., 2010).
Notably limiting the ability of marmots to gain mass is when they are
born their first year and when they reproduce the years after.
Individuals that are born later are less likely to survive overwinter
than those born earlier in the season (Monclús et al. , 2014).
Similarly, if a female is investing energy and resources into lactating
late into the season, she may also have a harder time surviving
overwinter than those that invest earlier (Andersen et al. ,
1976). We might assume that marmots should emerge and reproduce earlier
to increase the length of this crucial growing season. However, emerging
and reproducing too early also poses problems. If there is still snow on
the ground covering food resources when marmots emerge, they must draw
on depleted energy stores for longer (Cordes et al., 2020). This
could potentially lead to starvation, decrease the number of pups in a
litter, or cause marmots to forgo reproduction altogether (Inoyueet al., 2000). Nevertheless, there has been a documented advance
in the emergence date from hibernation (Edic et al., 2020).
Since marmots are thought to reproduce immediately following emergence,
we expected the timing of reproduction, pup emergence date, and adult
emergence date to be strongly linked and to follow a similar pattern.
However, how the timing of reproduction varies from year to year and the
impact of climate change on the timing of reproduction remains unknown.
Therefore, we were interested in examining whether the timing of
reproduction is changing in response to changes in average spring
temperatures and average spring snowpack. Given that these changes can
occur through microevolution and/or phenotypic plasticity, we further
investigated the relative contributions of each by examining whether the
trait is heritable, whether there is selection on the timing of
reproduction in response to climate change, and whether there is
phenotypic plasticity in the trait in response to changes in both
average spring temperature and snowpack. As reproduction is expected to
occur immediately following adult emergence, we expected the results for
the timing of reproduction and adult emergence to be similar. Therefore,
following Edic et al. (2020), we expected there to be low, but
estimatable heritability for the trait, strong plasticity, and an impact
of both spring temperature and snowpack. We further expected IxE in
plasticity and stabilizing selection on the timing of reproduction.
Methods: