Introduction
Animals exhibit great variation in coloration both within and among
species. Which colors persist and how these colors are arranged reflects
an optimization of competing adaptive functions including sexual
selection, thermoregulation, and camouflage (Walsberg et al. 1978,
Endler 1981, Andersson 1994, Stuart-Fox et al. 2017). Often, coloration
covaries with the environment when the adaptiveness of coloration
depends on how color and environment interact to influence individual
fitness (Cott 1940, Cuthill et al. 2017, Barrett et al. 2019). Over
evolutionary time, spatial and temporal changes in environmental
conditions can produce multiple color phenotypes in a population, or
color polymorphisms (Bell 2010, McLean and Stuart‐Fox 2014). Stable
color polymorphism is defined as the persistence of intraspecific
variation in coloration between sympatric individuals of the same age
group that is genetically inherited and the expression of which is not
sensitive to changes in body condition, diet, or environment (Huxley
1955, Roulin 2004). Color polymorphism occurs across a myriad of
vertebrates (e.g., mammals, reptiles, and birds) and is considered
essential for enabling species to respond to environmental gradients
associated with habitat type (Hoekstra et al. 2004), vegetation cover
(Baling et al. 2020), weather (Galeotti et al. 2009), and pollution
(Kettlewell 1955, Bishop 1972).
In high-latitude ecosystems, winter is characterized by freezing
temperatures and snow cover, a seasonal and dynamic environmental
feature that is important habitat for winter-adapted species. Snow has
implications for enhancing crypsis for polymorphic species and species
that exhibit seasonal coat color change. Twenty-one species of birds and
mammals exhibit seasonal molt changes from brown to white during the
winter allowing for greater camouflage on the snowy landscape (Grange
1932, Cott 1940, Mills et al. 2018). This phenotypic trait is an
adaptation to seasonal snow cover duration with potentially strong
fitness consequences. In some cases, when the rate of seasonal molt
change no longer matches the rate of snow cover change, a phenological
mismatch occurs. For example, seasonally molting rock ptarmiganLagopus mutus and snowshoe hares Lepus americanus that are
phenotypically mismatched with a snowless environment (due to the loss
of snow cover) exhibit lower survival during the winter months (Wilson
et al. 2019, Melin et al. 2020). This phenotypic mismatch between white
body coloration and snowless habitat has potentially strong implications
for population persistence, especially along southern range boundaries
where climate change-induced snow loss is shortening snow season length
and increasing periods of mismatch (Montgomerie et al. 2001, Mills et
al. 2013, Wilson et al. 2019). Similarly, for species that do not
undergo seasonal molts, environmental gradients (e.g., precipitation,
land cover), and periods of rapid environmental change are thought to be
maintaining forces for color polymorphism (Galeotti and Sacchi 2003,
Roulin 2004). For example, variability in annual snowfall and
temperature is likely an important selective force on plumage
polymorphism in the tawny owl Strix aluco , where survival of the
gray morph is higher than that of brown morphs during snowier winters
(Galeotti and Cesaris 1996, Karell et al. 2011).
The ruffed grouse Bonasa umbellus is a winter-adapted galliform
that occupies young forest across North America (Rusch et al. 2020) and
is polymorphic with two predominant color morphs of red or gray,
although intermediates frequently occur (Bump et al. 1947, Rusch et al.
2020). The genetic basis of color morphs in ruffed grouse has not been
described, though it is thought to be a melanin-based genetic color
polymorphism, which is the basis for red/brown polymorphisms across most
bird species (Roulin 2004, Mundy 2005). Throughout their range, the
survival rates of ruffed grouse vary seasonally and geographically
(Devers et al. 2007, Zimmerman et al. 2007, Wilson et al. 2022), but
little research has investigated possible demographic differences
between grouse color morphs. Winter is an important demographic
constraint for grouse populations in the upper midwestern United States
where mortality, mostly due to predation, is highest during the winter
months (Small et al. 1991, Gutiérrez et al. 2003, Pomara and Zuckerberg
2017). Ruffed grouse burrow in deep snow to evade predators and cold
ambient temperatures (Shipley et al. 2019, 2020, 2022), and overwinter
mortality is associated with shallow snow cover (Shipley et al. 2020),
but little is known about how phenotypic matching with snow might impose
differential survival for red and gray morphs.
Geographic clines in polymorphic traits can provide important insights
into the selective pressures that drive the persistence of polymorphism
as an adaptive strategy (Levins and MacArthur 1966, Takahashi 2015). For
ruffed grouse, it has been suggested that there is geographic variation
in color morph ratios across their range that covaries with latitude and
winter conditions, although this has not been formally described (Bump
et al. 1947, Rusch et al. 2020). Past authors have speculated that red
and gray morphs are differently sensitive to snow cover; suggesting that
there may be higher proportions of gray individuals found at more
northerly latitudes whereas red individuals are more associated with
southerly and coastal areas with lower snowfall (Gullion 1984, Rusch et
al. 2020). There is some evidence to suggest daily ruffed grouse
survival differs by season between morphs, but the relationship between
winter survival by morphs and snow cover has not been tested in
northern, seasonally dynamic ecosystems (but see: Gutiérrez et al.
2003).
Ruffed grouse occupy a range of different forest types and ages but are
closely associated with young successional forests (Zimmerman et al.
2009, Tirpak et al. 2010). The presence of young forest and dense cover
may offset the costs of phenotypic mismatches during winter. For
snowshoe hares, occupying patches of dense young aspen negated the
mortality associated with phenotypic mismatch (i.e., white snowshoe
hares on bare ground) (Wilson et al. 2019). In addition to this
potential buffering of phenotypic mismatch by forest cover, snow
presence and duration of seasonal snow cover varies across different
forest cover types (Petty et al. 2015). Forest canopy cover accounts for
57% and 72% of the variance in snow accumulation and ablation,
respectively (Varhola et al. 2010), and forest understory density can
alter ambient temperature and solar radiation that reaches the ground,
which in turn, alters snow cover depth and persistence (Lundquist et al.
2013, Petty et al. 2015).
Our goal was to examine phenotype-by-environment interactions between
color morph and snow cover and its role in mediating overwinter survival
in ruffed grouse. We used a five-year dataset of overwinter survivorship
for a population of ruffed grouse in central Wisconsin to investigate
potential effects of snow cover and habitat on individual survival of
ruffed grouse. We hypothesized that snow cover and habitat
characteristics would differently affect red and gray morph winter
survival. Under this hypothesis, we predicted that individuals who were
phenotypically mismatched to the surrounding winter landscape would have
lower survival. In other words, gray morphs would experience lower
survival during periods with less or patchier snow cover (Fig. 1).
Conversely, red morphs would experience lower survival during periods of
more persistent snow cover (Fig. 1). We further predicted that the cost
of phenotypic mismatch would be lower for individuals inhabiting areas
of dense cover such as young aspen forest (Wilson et al. 2019).