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\begin{document}

\title{Title: Evolution of breeding plumages in birds: A multiple-step pathway
to seasonal dichromatism in New World Warblers (Aves: Parulidae)}



\author[1]{Ryan Terrill}%
\author[2]{Glenn Seeholzer}%
\author[3]{Jared Wolfe}%
\affil[1]{Occidental College}%
\affil[2]{Louisiana State University}%
\affil[3]{Michigan Tech}%


\vspace{-1em}



  
  \date{June 18, 2024}


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\selectlanguage{english}
\begin{abstract}
Bird feathers serve multiple functions through their physical structure
and coloration, but the evolution of functional novelty in bird feathers
remains poorly understood. We investigated how selective pressures gave
rise to seasonal coloration change in the feathers of the New World
Warblers (Aves: Parulidae), a family with a remarkable diversity of
plumage, molt, and life history strategies. Seasonal color changes in
the plumages of migratory warblers are hypothesized to reflect a
tradeoff between natural and sexual selection on the breeding and
non-breeding distributions. We used comparative methods including
phylogenetic path analysis to examine nested hypotheses relating to the
evolution of seasonal dichromatism (i.e. breeding and nonbreeding
plumages) and the molts that produce these plumages. We found that
biannual molts likely evolved in response to increased feather wear and
that changes in feather coloration evolved after the biannual molt
itself. These results demonstrate that structural needs, not seasonal
selection on coloration, drive the evolution of molt strategies in
Parulidae. Importantly, once a biannual molt evolves, it served as a
preadaptation for seasonal changes in plumage color. These results
reveal how life history strategies act upon multiple and separate
feather functions to drive the evolution of feather replacement patterns
and bird coloration.%
\end{abstract}%



\sloppy


\textbf{Evolution of breeding plumage in birds: the relative influence
of life history, color change, and environment on the evolution of
biannual molt in the New World warblers (Aves: Parulidae).}

Abstract: Many species of birds show distinctive seasonal breeding and
nonbreeding plumages. A number of hypotheses have been proposed for the
evolution of this seasonal dichromatism, specifically related to the
idea that birds may experience variable levels of sexual selection
relative to natural selection throughout the year. However, these
hypotheses have not addressed the selective forces that have shaped
molt, the underlying mechanism of plumage change. Here, we examined
relationships between life-history variation, the evolution of a
seasonal molt, and seasonal plumage dichromatism in the new world
warblers (Aves: Parulidae), a family with a remarkable diversity of
plumage, molt, and life history strategies. We used phylogenetic
comparative methods and path analysis to understand how and why
distinctive breeding and nonbreeding plumages evolve in this family. We
found that color change alone poorly explains the evolution of patterns
of biannual molt evolution in warblers. Instead, molt evolution is
better explained by a combination of other life-history factors,
especially migration distance and foraging stratum. We found that the
evolution of biannual molt and seasonal dichromatism are decoupled, with
a biannual molt appearing earlier on the tree, more dispersed across
taxa and body regions, and correlating with separate life-history
factors than seasonal dichromatism. This result helps explain the
apparent paradox of birds that molt biannually but show breeding
plumages that are identical to the nonbreeding plumage. We find support
for a two-step process for the evolution of distinctive breeding and
non-breeding plumages: that prealternate molt evolves primarily under
selection for feather renewal, with seasonal color change sometimes
following later. These results reveal how life history strategies and a
birds' environment act upon multiple and separate feather functions to
drive the evolution of feather replacement patterns and bird coloration.

\textbf{Introduction}

When subject to dissimilar selective forces, traits that arose for one
function often diversify to serve another (Barve and Wagner 2013). Bird
feathers are as diverse in purpose as they are in form, reflecting
repeated evolution of novel functions since their origin in early
Archosauria (Dimond et al. 2011, Seebacher 2003). The array of feather
functions in birds is the product of separate, and potentially
competing, selective forces that have influenced the evolution of
feather structure and color over time (Dunn et al. 2015). Broadly,
feather diversity is shaped by natural selection imposed by
environmental conditions and by social selection (Dale et al. 2015, Lyon
and Montgomerie 2012). Selection often produces bright or gaudy plumages
in response to social competition (Rubenstein and Lovette 2009, Karubian
2002, S\selectlanguage{ngerman}ætre et al.1994, West-Eberhard 1979), while other selective
forces on feathers may enhance structural integrity for functions such
as flight and thermoregulation; or produce cryptic plumages to help
birds hide from their predators and prey. Selective forces vary
throughout a birds' annual cycle, and this variability has been
hypothesized to lead to the distinctive breeding and non-breeding
plumages shown by many species, \emph{i.e.} seasonal dichromatism
(Mulder et al. 1994). Plumage color change in birds has long interested
researchers (Holmgren and Hedenström 1995, Tökölyi et al. 2008, Simpson
et al. 2015, Beltran et al. 2018, McQueen et al. 2019), but much remains
to be discovered about the selective forces that shaped seasonal changes
in avian plumage coloration.

Feathers are lightweight and in order to maintain feather function, all
birds replace their feathers at least once per year through molt.
Without well-timed molts, birds can quickly lose functions of feathers
such as thermoregulation and flight. Seasonal dichromatism is commonly
acquired through biannual molts that produce plumages with disparate
phenotypes. While much study has focused on evolution of structure and
color in feathers (Prum 2005, Dale et al. 2015), our understanding of
the selective forces and evolutionary pathways which gave rise to
disparate molt patterns and strategies remains poor. The annual,
complete molt all birds undergo is termed the \emph{prebasic} molt, and
generates the \emph{basic} plumage. In addition to the prebasic molt,
many species of birds undergo a second molt within their annual cycle,
termed the \emph{prealternate} molt, which generates the\emph{alternate}
plumage and typically corresponds to what is colloquially known as the
breeding plumage (Wolfe et al. 2014). The prealternate molt varies
broadly in presence and extent among taxa, as well as the amount of
phenotypic change it produces. Many species of birds have alternate
plumages that are identical to their basic plumages, while others
exhibit markedly different alternate and basic plumages. Some are so
different that basic and alternate plumaged birds of the same species
were originally described as separate species,\emph{e.g.} Black-bellied
Plover (\emph{Pluvialis squatarola} ; Poole et al. 2016). Different
species of birds exhibit diverse molt strategies across the globe
(Stresemann and Stresemann 1966). What factors have influenced the
evolution of divergent molt strategies? When feathers are replaced more
than once a year, is this in response to needs to replace worn feathers,
or to grow feathers with a new phenotype?

Two hypotheses exist to explain the evolution of seasonal dichromatism
in birds. The first hypothesis, which we term the \emph{variable needs
hypothesis} , concentrates on feather color and states that prealternate
molt evolved in response to differential relative levels of social and
natural selection throughout the year (Tökölyi et al. 2008, Simpson et
al. 2015, McQueen et al. 2019). This hypothesis is based on the
observation that social selection for bright plumage is stronger during
the breeding season (Hill 1991, Karubian 2002, Butcher and Rohwer 1989),
and may be weaker outside the breeding season such that natural
selection would favor a more cryptic plumage in order to evade detection
by predators and prey (Götmark et al. 1997, Slagsvold et al. 1995).
Long-distance migrant birds experience a brief period of intense sexual
selection during the breeding season, which is likely reduced on the
non-breeding grounds; though male-male competition may play a strong
role in winter plumages in at least some species (Reudink et al. 2009).
There is evidence that this has likely led to a latitudinal gradient in
sexual dichromatism in the New World warblers and orioles (Friedman et
al. 2009, Hamilton 1995, Simpson et al 2015). On the other hand,
resident species may form pair bonds all year, and experience more
stable relative levels of sexual and nonsexual selection on feather
color throughout the year. Under this hypothesis, the prealternate molt
evolved similarly to sexual dichromatism -- for plumage color. This
hypothesis states that prealternate molt evolves in response to variable
needs for feather colors induced by changes in the relative strength of
sexual and natural selection on feathers throughout a birds' annual
cycle.

The second hypothesis, which we term the \emph{feather wear hypothesis}
, is focused on feather structure. It is based on an observation that
prealternate molts appear to be more common in long-distance migrants
than in non-migratory species and does not always produce plumage color
change (Fig 1). Pyle and Kayhart (2010) and Wolfe (2011) observed that a
prealternate molt that produces feathers with the same coloration as
prebasic molt is a widespread phenomenon in birds, and proposed that
prealternate molt mat not evolve for breeding plumage necessarily.
Instead, they proposed that prealternate molt evolves to replace worn
feathers, and then can be co-opted by pressures for seasonal
dichromatism. The idea that the realization of selection on plumage
color is limited by pre-existing molts is not entirely novel. Rowher and
Butcher (1988) investigated delayed plumage maturation in birds, and
found that molt limitations explained patterns of plumage color better
than explanations based on social selection alone. The \emph{feather
wear hypothesis} similarly views feather color development through the
lens of molt limitations, and proposes that the relationship between
long-distance migration and prealternate molt may be driven by the need
to replace feathers worn by ultraviolet radiation, where migration
degrades feathers through extended photoperiods experienced throughout
the year (Lennox and Rowlands 1969, Surmacki 2008). This idea is
supported by theoretical models demonstrating that biannual molt should
evolve when poor feather quality has elevated impacts on survival rates
(Holmgren and Hedenström 1995). Migrant breeders experience longer days
and increased feather wear through bleaching during their summer
breeding seasons at temperate latitudes relative to resident tropical
species (Fig. 1c.). Thus, the \emph{feather wear hypothesis} is that
prealternate molt evolved to replace worn feathers associated with a
migratory lifestyle and increased solar exposure during longer days, and
then functioned as preadaptation for the evolution of seasonal
dichromatism following the \emph{variable needs hypothesis} .
The\emph{feather wear hypothesis} does not rule out variable needs for
feather colors, but instead proposes a different mechanism for the
origin of prealternate molt. The feather wear hypothesis is a
multiple-step evolutionary process for the evolution of seasonal
dichromatism: prealternate molt evolved to replace feathers, and was
subsequently co-opted for seasonal dichromatism in response to
differential selective forces at different times of year.

We examined these two hypotheses using the ecologically diverse New
World Warbler (Parulidae) family, which exhibit remarkable variation in
plumage characteristics and migratory behaviors. Variation in molt
strategies in this family are accompanied by gains and losses in
migratory behavior (Winger et al. 2011) as well as considerable
variation in life history characteristics, making them a suitable system
to assess how interactions between separate selective forces influenced
the evolution of seasonal dichromatism. To test these hypotheses, we
quantified the extent of prealternate molt and seasonal dichromatism in
the New World warblers, as well as 31 life history and environmental
characteristics that may affect the evolution of prealternate molts and
plumage coloration through natural selection.

\textbf{Methods}

\emph{Molt and dichromatism scoring}

We scored the extent of prealternate molt and plumage dichromatism using
a combination of specimen examinations and literature review. All
specimens were examined at the LSU Museum of Natural Science. We used a
combination of collection date, data from specimen labels, and known
molt patterns (Pyle 2007) to classify individuals by age, sex, and molt
stage. Species or life stages not available at the LSUMNS were scored
from the literature (Pyle 2007) or visual examination of published
photographs of plumages (Dunn and Garrett 1997, Stephenson and Whittle
2013). We defined a dichromatic region as a region with visible color or
pattern differences between basic and alternate plumage. We scored
dichromatism in feather regions as follows: 1 = region completely
dichromatic, 0 = no dichromatism in region, and 0.5 = and partial
dichromatism or intraspecific variation. In some species, extent of molt
and dichromatism differs between the first prealternate molt and
definitive prealternate molts. In these cases, we considered only the
definitive prealternate molts (Wolfe et al. 2014). We scored molt extent
using the same museum and literature resources, through examination of
molt limits (Pyle 1997a). For each body region (Fig 2f), we scored molt
as follows: 1= complete replacement of the feathers in the region, 0 =
molt absent from the region, and 0.5 = either partial replacement of the
feathers in that region, or intraspecific variation in extent of molt.

\emph{Life history parameters}

A birds' lifestyle and environment likely affect needs for feathers, and
so we attempted to quantify many life history and environmental
parameters for each species. All calculations of life history and
environmental parameters were conducted in R version 3.3.1 (R Core team
2016). Spatial data were extracted using shapefiles of species
distributions provided by Birdlife International and NatureServ
(Birdlife International 2016). We worked with the shapefiles of spatial
distributions of Parulidae using the packages GISTools (Brunsdon and
Chen 2014), maptools (Bivand and Lewis-Koh 2016), raster (Hijmans 2016),
and geosphere (Hijmans et al. 2005) in R. We chose to quantify life
history and environmental parameters that reflect factors that may
result in feather wear from solar exposure due to distribution and
migratory behavior, as well habitat use and foraging stratum. These
parameters are migratory distance, breeding latitude, wintering
latitude, day length experienced throughout the year, breeding and
winter habitat, breeding and winter foraging stratum, nest type,
intensity of solar radiation experienced over the year, intensity of
solar radiation experienced in the breeding and wintering range
(separately), and precipitation, minimum maximum and mean temperature,
and elevation, on the breeding and wintering ranges, separately. We also
calculated body mass. Below, we detail how we measured or scored these
parameters.

\emph{Migratory distance and Latitude}

To estimate migratory distance, we divided species into three
categories: Migrants, which have no spatial overlap between their
breeding and nonbreeding distributions; non-migrants, which have
complete overlap between breeding and nonbreeding distributions, and
partial migrants, which have some overlap between breeding and
nonbreeding distributions. Non-migrants were always set to zero
migratory distance. Using shapefiles of breeding and non-breeding
distribution (Birdlife 2016) we calculated six separate estimates of
migratory distance: 1: distance between the mid latitudes of each
distribution, 2 \& 3: distance between the maximum and minimum latitudes
of each distribution respectively, 4: distance between maximum latitude
of breeding distribution and minimum latitude of nonbreeding
distributions, 5: distance between minimum latitude of the breeding
distribution and maximum latitude of the nonbreeding distribution, and
6: the great circle distance between the centroids of the points. We
used linear models to examine the autocorrelation between these
variables and chose the first measure of migratory (distance between
mid-latitudes) distance to use in further analysis, because it best
predicted the other measurements of migration. We calculated the
latitude of the breeding and winter ranges of each species as the mean
latitude value of each shapefile.

\emph{Solar Radiation, Day Length, and Climate Variables}

We calculated solar radiation, day length, temperature, precipitation,
and elevation values for each species by extracting spatial data from
the distribution shape files used to calculate migratory distance. Data
were extracted separately for breeding (May-July) and non-breeding
(Nov-Feb) seasons. Although nonbreeding and partial migrant birds may
reside in the same location for 12 months, we extracted values from the
same periods for all species for consistency. The solar radiation and
day length datasets were acquired from the NASA Langley Research Center
Atmospheric Science Data Center Surface meteorological and Solar Energy
(SSE) web portal supported by the NASA LaRC POWER Project (Nasa 2008).
We estimated radiation as the average insolation incident on a
horizontal surface per month (hereafter solar radiation) over the course
of a year in units of kWh/m\^{}2/month. We estimated daylight hours as
the average daylight hours a species experiences per month (hrs/month).
We separated solar radiation into radiation experienced in the breeding
and winter ranges separately and combined for an overall average. We
also created a new variable to estimate total solar exposure by
multiplying solar radiation by day length. We extracted ten climatic
variables from WorldClim 1.4 (Hijmans et al. 2005) at 2.5 minutes
resolution. We extracted breeding and nonbreeding range values from
maximum, minimum, and mean temperature, precipitation, and altitude data
sets. Temperature is provided and degrees Celsius x 10. To extract solar
radiation, day length, and climate variables, we generated 10,000 points
randomly within each distribution map polygon. We extracted data from
each variable layer at each of the 10,000 points for the breeding and
winter months, in the appropriate polygon for each species. We then
calculated the mean value for each variable in the breeding and winter
distributions.

\emph{Habitat and Stratum}

We created a scoring system for habitat and stratum that roughly
estimated solar radiation exposure by species. We scored habitats using
the following codes: 0 = tall deciduous forest, 1 = coniferous/montane
forest, 2 = riparian/secondary/gallery forest, or broad forest type use,
3 = stunted/young forest, 4 = forest edge, 5 = scrub/marshes, 6 = open
habitat. We rated stratum by relative stratum within a habitat using the
following codes: 0= ground or near ground. 1= understory/undergrowth, 2
= midstory, 3= subcanopy, 4 =canopy/edge/open. Using data from Dunn and
Garrett (1997), Curson (2010), Stevenson and Whittle (2013),
Rodewald\textsuperscript{(}2015) and Schulenberg (2019) we scored the
habitat and foraging stratum during the breeding and wintering periods
for each species. We also scored the stratum of nest placement and the
nest type from these sources. We coded nest types as the following: 0 =
cavity, 1 = dome/closed, 2 = open cup.

\textbf{Analysis}

We conducted all phylogenetic analyses using a recent, multilocus
phylogeny of the Parulidae (Lovette et al. 2010).

\emph{Model Selection and Phylogenetic Signal}

We fit models of evolution to molt and dichromatism to understand how
phylogenetic history and selection may interact with these traits, as
well as to inform phylogenetic comparative analyses involving these two
traits. To select models of evolution for molts and dichromatism, we fit
various models of evolution to the data and phylogeny. We fit models of
character evolution using Brownian motion (BM), Orstein-Uhlenbeck (OU),
and Early-burst (EB) (Butler 2004) models in the package geiger in R
(Harmon et al. 2008). We fit models of continuous traits for feather
regions and extent of molts and dichromatism, and models of discrete
traits for presence of molts and dichromatism. We extracted the sample
size-corrected AIC (AICc) values and parameters from the BM, OU, and EB
models for cross-model comparisons and converted these values to AIC
weights to compare models (Revell 2012). We compared the AICc weights
for these three models by calculating AICc weights for each feather
tract and for presence and extent of prealternate molt, and seasonal
dichromatism. To assess the best model across body regions, we
calculated AICc weighted parameter values across feather regions by
weighting rate parameters by AICc weights and summed these weighted
parameters for molts and dichromatism. We calculated phylogenetic signal
as Pagel's Lambda in phytools (Revell 2012) for each molt and sexual and
seasonal dichromatism for each body region, as well as presence and
extent of molts and dichromatism.

The difference between gains and losses of traits can be important to
understand how traits change and interact over evolutionary time. We
were interested in knowing when and how often seasonal dichromatism and
prealternate molt were gained and lost, and whether these transitions
provided insight into the relationship between prealternate molt and
seasonal dichromatism. We evaluated the number of transitions and the
probability that rates of gains and losses were significantly different
for presence of molts and dichromatism by reconstructing ancestral
states under equal rates (ER) and all rates different (ARD) models; we
compared the log-likelihoods of each model using a likelihood ratio test
to obtain a p-value for rejection of the ER model in favor of the more
complex ARD model. This method allowed us to ask if rates of gains and
losses of molts and dichromatism were significantly different from
equal. We used a similar test, based on Pagel (1994) to test if the
evolution of prealternate molt is dependent on long-distance migration,
through comparison of likelihood ratios of dependent and independent
models of evolution (Figure 1g).

\emph{Ancestral State Reconstruction and Rates of Evolution}

To understand the evolutionary history of prealternate molt and seasonal
dichromatism, among separate species and feather regions, we constructed
ancestral state estimates of molts and dichromatism as discrete
variables by feather region (Figure 4). We conducted ancestral state
reconstruction of presence of molts and dichromatism on the whole body,
and by feather region. To convert continuous characters to presence, we
converted any nonzero integer to a 1, to indicate that the molt or
dichromatism is present in the region of interest. We then evaluated the
probability of presence and absence of molts and dichromatism for the
entire body and by feather region at each node using a likelihood
framework in the package APE (Paradis et al. 2004) in R. We conducted
model testing by reconstructing ancestral states under both equal rates
(ER) are all-rates-different (ARD) models and used likelihood ratio
tests to choose the best model with which to reconstruct ancestral
states to help us understand whether we were correctly evaluating the
rates of gains and losses over time. We also evaluated molts and
dichromatism as continuous characters, scored as the number of feather
regions involved, and reconstructed their ancestral states to evaluate
their ancestral states and rates of evolution as continuous characters
across the bodies of these birds.

\emph{Phylogenetic mixed models for molt and dichromatism extents}

We built phylogenetic mixed models to predict the presence and extent of
prealternate molt and seasonal dichromatism to understand the relative
influences of life history and environmental variables on these traits.
To build mixed models of exogenous correlates of molt extents, we first
conducted pairwise phylogenetic generalized least squares analysis over
extents of molt, dichromatism, and exogenous correlates (extended data
table 1) using the package caper (Orme et al. 2013) in R. We examined
pairwise PGLS results for strength and significance of interactions and
used these interactions to build sets of mixed models to test for the
effects of exogenous drivers on extents of molts and dichromatism by
examining pairwise interaction between molts, dichromatism, and
ecological data, as well as covariation between life history and
ecological correlates. We evaluated these mixed models using caper,
MuMIn \textsuperscript{(}Barton 2016) and Nlme (Pinheiro et al. 2016) in
R, and organized the models using information theory by ranking models
by their AICc score (Table 1).

\emph{Phylogenetic ANOVA of drivers of molt and dichromatism in feather
regions}

Identifying those feather regions being replaced by the prealternate
molt can provide clues as to why this molt evovles To investigate how
migratory distance interact with molts and dichromatism within
individual feather regions, we conducted a phylogenetic-controlled
analysis of variance (ANOVA), for each feather region using the package
phytools (Revell 2012) in R. We investigated the influence of migratory
distance on prealternate molt within feather regions by comparing these
continuous characters to presence and absence of prealternate molt (Fig.
2g). We then conducted Holm's sequential Bonferroni post-hoc tests on
the phylogenetic ANOVA results to correct for simultaneous test runs.

\emph{Phylogenetic path analysis}

Because the \emph{feather wear hypothesis} is a multiple-step
hypothesis, it is important to be able to parse direct and indirect
relationships between variables. We investigated these direct and
indirect relationships using a phylogenetic path analysis, following the
method outlined by and von Hardenbeg and Gonzalez-Voyer (2016) as
explained in Garamszegi, Ed. (2014). Phylogenetic path analysis has
several advantages when assessing multivariate relationships, especially
in its ability to discriminate between direct and indirect effects
between variables, and in its consideration of multiple interactions at
once. To evaluate the multivariate interactions in this system, we used
results from PGLS analyses to inform 12 separate hypotheses of direct
and indirect effects within prealternate molt, seasonal dichromatism,
migration distance and foraging stratum (supplemental fig. 1). We used a
d-sep based path analysis to build sets of phylogenetic-controlled model
equations, which we evaluated using the package caper (Orme et al. 2013)
in R. We then used an information theory approach based on a C statistic
(Sjipley 2016) to rank candidate models. The C-statistic evaluates ranks
the conditional independencies within the models and produces
CIC\textsubscript{c} score for each model. We used P-values and CICc
(Von Hardenberd and Gonzales-Voyer 2013) scores to evaluate the
probability and information content of the C-statistic, respectively. We
used P-values of the C statistic to identify a subset of models that we
were not able to reject, and then ranked models by their CICc score to
evaluate the likelihood of each candidate model.

\textbf{RESULTS}

\emph{Ancestral State Reconstruction}

We found support for an Ornstein-Uhlenbeck (OU) model (AICc weight =
.96), for presence of prealternate molt, but support for Brownian motion
(BM) evolution (AICc weight = .60) for extent of prealternate molt. We
found support for a BM model for both presence (AICc weight = .56) and
extent (AICc weight = .57) of seasonal dichromatism.

The feather regions more involved in prealternate molt, namely the head,
breast, belly, and back, showed higher rates of evolution relative to
other feather regions (Fig. 4). We reconstructed a partial prealternate
molt at the root of the tree, only on the head, with no associated
seasonal dichromatism, and several gains and losses of both seasonal
dichromatism and prealternate molt (Fig. 4), which agrees with our
transition analysis (Fig. 1) that prealternate molt can be gained and
lost over time, over separate lineages (Fig. 1e).

\emph{Phylogenetic generalized linear models assessing exogenous
correlates among extents of molts and dichromatism}

For individual pairwise comparisons between variables, we found that
extent of seasonal dichromatism was best predicted by extent of
prealternate molt (adjusted R\textsuperscript{2}= .312,
p\textless{}.001), and day length (adjusted R\textsuperscript{2}= .065,
p=.046), and migration distance (adjusted R\textsuperscript{2}= .072, p
=.039) which were correlated with prealternate molt. Seasonal
dichromatism was also significantly correlated to foraging stratum
(adjusted R\textsuperscript{2}= .078, p=.032), which was not correlated
with prealternate molt. The extent of prealternate molt was
significantly correlate with extent of seasonal dichromatism (adjusted
R\textsuperscript{2}= .312, p\textless{}.001), day length (adjusted
R\textsuperscript{2}= .16, p = .001), migration distance (adjusted
R\textsuperscript{2}= .188, p = .013), and breeding latitude (adjusted
R\textsuperscript{2}= .109, p = .013); figure 1).

16 mixed models significantly predicted the extent of prealternate molt
with significance of p\textless{}.05, and we ranked these models using
the sample size-adjusted information theory criterion
AIC\textsubscript{c}(Table 1). The top model for extent of prealternate
molt outperformed all other models by a sizable margin, and the top two
models combined accounted for the majority of the AIC weight. Top models
that predicted the extent of prealternate molt generally included day
length, solar radiation both in the breeding and nonbreeding season, and
migratory distance as predictor variables. In all, we found fifteen
models that predicted the extent of seasonal dichromatism with
significance of p\textless{}.05; and these models included the extent of
prealternate molt, foraging stratum both in the breeding and nonbreeding
season, and migratory distance (Table 1). Top models were evaluating
seasonal dichromatism more evenly weighted than models for prealternate
molt, with the top two models produced similar
AIC\textsubscript{c}values, and the third and fourth models produced
similar AIC\textsubscript{c} values. All four of these top models, which
accounted for the majority of the AIC\textsubscript{c} weight, included
extent of prealternate molt and foraging stratum. Foraging stratum, both
in the breeding and nonbreeding season, was the main predictor variable
in the top models for the extent of seasonal dichromatism that was not
associated with top models of prealternate molt.

\emph{Phylogenetic ANOVA of feather regions}

We found a that the positive correlation between migratory distance and
prealternate molt was repeated across feather regions. In general,
migratory distance predicted whether a feather region was replaced
during prealternate molt (Fig. 2). This relationship was significant in
the head (F = 13, p=.002), breast (F=15.5,p=.001), back
(F=12.47,p=.033), belly (F=14.8,p=.013), and tertials (F=11.1,p=.015).

\emph{Phylogenetic path analysis}

Two path models were strongly favored by information theory analyses,
with roughly equivalent CICc values. These were models 2 and 3 (fig. 4),
both of which proposed that prealternate molt and foraging stratum are
direct parent variables of seasonal dichromatism and that migration
distance is a direct parent of variable of day length, and only differed
in whether migration distance or day length was a direct parent of
prealternate molt. The best model that proposed a conditional
independency for prealternate molt was model 5, the next best model
after models 2 and 3, though this model showed a marked jump in its CICc
value compared to models 2 and 3. (fig. S2).

\textbf{Discussion}

\emph{The feather wear vs. variables needs hypotheses}

The \emph{variable needs hypothesis} , which proposes that prealternate
molt evolves in response to birds' needs to change colors, predicts
coevolution of prealternate molt and seasonal dichromatism. We found
discrepancies in the best fit models of evolution, timing, pattern and
external correlates of evolution of between the prealternate molt and
seasonal dichromatism. The character that we studied with the strongest
evidence for selection, as interpreted by the ratio of likelihood for an
Ornstein-Uhlenbeck model to a Brownian Motion model, was presence of
prealternate molt. This may imply that prealternate molt itself is under
stronger selection (Butler and King 2004) than the color change it
produces, which fit slightly better to a model of Brownian motion. We
interpret this as support for the \emph{feather wear hypothesis} ,
because this hypothesis predicts stronger selection on molt patterns
than on seasonal dichromatism. The life history characteristics that
best predicted prealternate molt were migration distance, day length,
and solar radiation experienced on the breeding grounds (Fig 1, table
1). Top models for seasonal dichromatism all included prealternate molt
and foraging stratum on the breeding and nonbreeding ranges. Combined
with the results of the path analysis, we interpret these results as
evidence for prealternate molt and seasonal dichromatism evolving along
separate pathways.

The \emph{feather wear} hypothesis invokes preadaptation in the
relationship between prealternate molt and seasonal dichromatism.
The\emph{variable needs hypothesis} may predict synchronous evolution of
prealternate molt and seasonal dichromatism, whereas the \emph{feather
wear hypothesis} predicts that prealternate molt should precede seasonal
dichromatism and correlate with separate external parameters When we
investigated the evolutionary timing of these characters, prealternate
molt appeared to arise before seasonal dichromatism, and in more species
and feather regions (Fig. 4). The idea that a character can evolve in
response to selection for one function, and then be co-opted to serve
another, has been well-explored in evolutionary biology (Bock 1959).
Preadaptation has been implicated in the evolution of a wide array of
evolutionary novelties (Cheney and Seyfarth 2005, Ketola et al. 2013,
Schiestl and Cozzolino 2008, Quiñones and Pen 2017), and is an important
phenomenon to understand when investigating how traits evolve. Our
ancestral state reconstruction suggests that prealternate molt is a
preadaptation, rather than an adaptation for seasonal dichromatism. We
do not present these results as a rebuttal to variable needs for feather
color. Clearly, needs for feather colors vary with life-history and
latitudinal gradients in social behavior (Friedman et al. 2009), needs
for crypsis on migration (Simpson et al. 2015) and nest stratum (Martin
and Badyaev 1996), though we found little support for a relationship
between nest stratum or nest type and prealternate molt or seasonal
dichromatism. Our findings suggest that latitudinal gradients likely do
play a role in the evolution of color change in feathers once
prealternate molt is present. From these results, we propose a two-step
pathway for the evolution of disparate breeding and nonbreeding plumages
in warblers: a biannual molt evolves in response to structural needs for
feathers, and then serves as a preadapted mechanism for seasonal
dichromatism.

Immediacy of needs helps explain why structure may influence molt more
than needs for color change. Structural functions provided by feathers
are more immediately necessary for survival of birds than colors that
function for social signaling. Without feathers, chicks are
poikilothermic (Whittow and Tazawa 1991) and reliant on their parents
for warmth. In adult birds, worn feathers directly influence survival
through decrease of important functions such as flight (Swaddle et al.
1996). Timing of molt appears to be so important that experimentally
malnourished birds will undergo a molt in spite of losing up to 40\%
body mass in the process, instead of delaying molt (Murphy et al. 1988).
Because of more immediate implications on survival, it may make sense
that selection on feather structure is stronger than on color change,
and that selection on feather structure may be more likely to influence
the evolution of molt strategies.

\emph{Life History and Environmental correlates of molts and color
change}

Phenotypic evolution is the result of repeated interactions between
selective pressures and pre-existing structures available for selection
to act upon, in addition to neutral drift. While Gould and Lewontin
(1979) has been widely criticized for oversimplifying adaptation
hypotheses (Pigliucci and Kaplan 2000), a general point that it explains
well is that selection can only work upon biological features that
exist, and that contemporary uses for a biological structure may not
fully explain why that structure originally evolved. While it may make
intuitive sense that prealternate molt is ``for'' a breeding plumage,
and indeed some naming conventions (\emph{e.g.} prenuptial molt,
prebreeding molt) imply this causative relationship; it is important to
disentangle direct and indirect causation when attempting to understand
how selection interacts with phenotypic evolution over time (Hardenberg
and Gonzalez-Voyer 2013). Phylogenetic path analysis produced two top
models, both of which found that the extent of prealternate molt was
driven directly by migratory distance and cumulative annual day length..
This suggests that seasonal dichromatism is connected indirectly to
migratory distance through prealternate molt (Fig 3b). The models
suggested that seasonal dichromatism was determined by the presence of
the prealternate molt and foraging stratum, with birds foraging in more
open strata experiencing more extensive prealternate molts and seasonal
dichromatism. This generally agrees with previous findings that sexual
selection operates more strongly in canopy birds, which tend to be more
visually oriented (Gomez and Théry 2004, Shutler and Weatherhead 1990),
resulting in brighter plumages (Shultz and Burns 2013). From a
structural standpoint, canopy birds may also experience greater solar
exposure. Indeed, one of the few tropical groups of birds with a known
prealternate molt are the becards (\emph{Pachyramphus} ; Johnson and
Wolfe 2018) which show identical alternate and basic plumages, and
inhabit canopy and forest edge habitats. Importantly, breeding season
foraging stratum, when combined with extent of prealternate molt,
strongly predicted extent of seasonal dichromatism, but did not by
itself predict extent of prealternate molt (table 1). This suggests that
selective pressure on plumage color acts on seasonal dichromatism only
after prealternate molt has evolved for other reasons and then provides
a structural canvass for sexual selection to paint upon.

Past studies have found that sexual dichromatism can evolve through the
loss of a gaudy plumage among female migratory birds (Simpson et al
2015). Similarly, we find that at least in some cases, year-round
monochromatism evolved through loss of the prealternate molt. It is
important to consider phylogenetic context in the evolution of different
types of dimorphism because trait gains and losses may mean different
things over evolutionary time. For example, Simpson (2015) found sexual
dichromatism in warblers stems from loss of bright coloration in
females, and Hoffmann et al (2009) found a similar pattern in oriole
plumage. From the perpsective of migratory distance, Winger and Lovette
(2011) showed that resident warblers were more likely to be examples of
lineages that had lost long-distance migration. We found gains and
losses of both seasonal dichromatism and prealternate molt, and,
importantly, we found that losses of long-distance migration were
associated with loss of prealternate molt. Froelich et al. (2005) and
Tökölyi et al. (2008) proposed that the relationship between migratory
distance and seasonal dichromatism is caused by earlier breeding in
resident species which limited their ability to molt; however, resident
species do not appear to be limited in their molts when compared to
migrant birds, as they show increased molt-breeding overlap (Johnson et
al. 2012) and protracted molts (Kiat et al. 2019, Terrill 2018).
Furthermore, it is likely that migrant birds are limited in their molt
timing, as they generally complete prealternate molt before beginning
spring migration (Pyle 1997b). Without a prealternate molt, nonmigratory
warblers are often the same color throughout the year, and resident
warblers fall into two categories, those that are either gaudy all year,
or cryptic all year. These findings suggest that variable needs for
feather color alone are not strong enough to maintain a biannual molt in
these birds, without an external force acting on the structural
integrity of their feathers, and long-distance migration directly
impacts structural integrity. Furthermore, pressures that affect the
latitudinal gradients in sexual dichromatism and seasonal dichromatism
likely differ because each is derived from a different mechanism. While
sexual dichromatism can be associated with the \emph{prebasic} molt and
result in a year-long plumage aspect, seasonal dichromatism results in
discrepancies between the \emph{prebasic} and \emph{prealternate} molt,
and results in seasonally variable plumage aspects.

\emph{Molt and coloration across feather regions}

Selective pressures on plumage may vary across birds' bodies (Marcondes
and Brumfield 2018, Dale et al 2015). We know that molt in different
species of birds varies in which feathers are molted and when
(Stresemann and Stresemann 1966), but, despite some hypotheses being put
forward (Howell 2010), little work has investigated the interplay
between feather function and molt patterns across feather regions. Among
species of warblers, certain feather regions were repeatedly more or
less likely to be involved in prealternate molt. Despite variation in
prealternate molt extent, ancestral state reconstruction suggested that
the prealternate molt evolved in a stereotyped manner (Fig. 2g; Fig. 4).
The head is involved in prealternate molt in all species, amnd then most
frequently followed by the back, breast, belly feathers and wing
coverts. Prealternate molt rarely replaces other parts of the body,
including wing and tail feathers, which are often shaded from the sun by
covert feathers and each other. The feather regions more involved in
prealternate molt appear to be those more exposed to the sun on a
perched bird (Fig 2f). Although the wing and tails are prominent
features on birds, when folded, each individual remex is almost entirely
shaded by coverts and other remiges. (Fig. 2). It may also be the case
that the larger and stronger remiges are costlier to replace than body
feathers, but we interpret this evidence as at least suggestive that
feathers that are more exposed to the sun are more likely to be replaced
in prealternate molt. This pattern was confirmed by both ANOVA analysis
and ancestral state reconstruction, where feather regions most strongly
associated with prealternate molt were also correlated with
long-distance migration (Fig 2g, Fig. 4), and showed increased rates of
evolution in seasonal dichromatism and prealternate molt (Fig. 4). In
each feather group, we recovered the same positive relationship between
migratory distance and likelihood of replacement in prealternate molt
(Fig. 2g). We found gains and losses of long-distance migration and
prealternate molt; and, importantly, found no gains of prealternate molt
in birds without long-distance migration, but a high transition rate to
prealternate molt in lineages with long-distance migration (Fig. 1g).
The predictable evolution of prealternate molt in regions of the body
more exposed to the sun, coupled with a lack of seasonal dichromatism in
lineages which recently evolved prealternate molt, lends support to the
feather wear hypothesis for the evolution of prealternate molt.

\emph{Feather wear and structural needs}

Photodegradation is a primary source of feather structure atrophy in
feathers (Ito et al. 2017, Pearlstein et al. 2014). The main variables
that predict extent of prealternate molt are migration distance, day
length, and foraging stratum. Migration distance likely affects feather
degradation through increased overall day length (Fig. 1a).
Long-distance migrants experience longer days overall because they
experience long summer days in the temperate zone, but escape short
winter days. For example, the longest-distance migrant in our dataset,
and one of the most seasonally dichromatic species with one of the most
extensive prealternate molts, the Blackpoll Warbler (\emph{Setophaga
striata)} experiences an average of 1.7 more hours of daylight each day,
or 621 more hours of ultraviolet exposure each year, when compared to
the species exposed to the least amount of ultraviolet radiation, the
Masked Yellowthroat (\emph{Geothlypis aequinoctialis} ), which also
shows no seasonal dichromatism and no prealternate molt. Additionally,
many warbler species exhibit prealternate molts that do not result in
seasonal dichromatism, this phenomenon may seem paradoxical from the
standpoint of hypotheses focused on coloration as the evolutionary
catalyst for the prealternate molt, but makes sense within the context
of the \emph{feather wear hypothesis.}

Evidence from other taxa outside the New World Warblers provides
additional context for the relationship between prealternate molt and
seasonal dichromatism. The most extensive prealternate molts in birds
occur in three species of long-distance migrants that breed, winter, and
migrate in open, solar-exposed environments: Franklin's Gull
(\emph{Leucophaeus pipixcan} ; Howell 2010\emph{)} , Bobolink
(\emph{Dolichonyx oryzivorus} ; Renfew et al. 2011\emph{)} and Willow
Warbler (\emph{Phylloscopus trochilus;} Underhill et al. 1992\emph{)} .
Bobolink shows seasonal change in feather color, but Willow Warbler does
not, and Franklin's Gull only shows a partial plumage color change. In
these species, anecdotally, migration distance and habitat better
predict prealternate molt than color change. The Willow Warbler is an
extreme example: this species completely replaces all feathers twice a
year, but the basic and alternate plumages are indistinguishable.
Further research into this phenomenon should expand beyond the new world
warblers to other groups of birds, as well as attempt to measure
relative feather degradation rates in association with life history,
habitat, and environment in birds, and study groups with more variable
social systems. Other resident species of birds with strong variable
selection on feather color, such as Ptarmigans (Beltran et al. 2018) may
indeed have molts that evolve solely for variables needs of feather
color. Overall, our results demonstrate the importance of molt
strategies in the functional diversification of feathers and illuminates
the value of considering interactions between different functional
requirements for birds in the evolution of feather function.

\textbf{Conclusions:}

Based on the observation that prealternate molt often involves feathers
that appear to be identical between basic and alternate plumage, Pyle
and Kayhart (2010) proposed that prealternate molt may evolve to replace
sun-exposed feathers, then later be co-opted for seasonal dichromatism.
We examined this hypothesis across warblers and found that it better
explains patterns of evolution of prealternate molt than color change
alone. Here, we present evidence that selection on coloration and
structure interact in complex ways to influence the evolution of molts
and plumages in warblers. Namely, we find that color change poorly
explains the evolution of the molts that produce these changes. This
suggests that biannual molt acts as a preadapted platform for color
change, instead of evolving in direct response to needs for color
change. These results provide a more nuanced understanding of plumage
evolution in birds by incorporating the mechanism for plumage
generation. Rohwer and Butcher (1988) made a novel contribution to our
understanding of delayed plumage maturation in birds by arguing that
molt must be understood first in order to understand plumage maturation
in birds. They found that the breeding-season driven hypotheses lose
support when molt is studied, and that the limitations of preexisting
molts explain delayed plumage maturation in birds better that social
selection on the breeding grounds. Our results largely agree with this
study, in that we find needs for plumage change do not appear to be able
to influence the evolution of molt strategies, instead they only
influence the phenotypes of feathers produced within molt strategies
that have evolved for other reasons. Similarly, needs for seasonal color
change may be present in species, but the translation of that need into
phenotype may be limited by the extent of prealternate molt. Following
our results and those of Rohwer and Butcher (1988) that hypotheses about
the role of social selection on feather color may look different when
viewed through the lens of molt, we encourage other authors studying the
evolution of plumage to consider molt strategies when attempting to
understand mechanisms of feather evolution.

Feather color has attracted much attention, especially into selective
processes that may have produced the diversity of coloration present in
birds' feathers (Darwin 1871, Wallace 1891, Chaine and Lyon 2008, Li et
al. 2010, Payne 1984). Both natural and sexual selection play roles in
the colors of feathers as well as diversification of birds (Barraclough
et al. 1995, Møller and Cuervo 1998, Stoddard and Prum 2007, Marcondes
and Brumfield 2019). However, the molts that produce these feathers have
been largely ignored in these studies. Birds show a diverse array of
molt strategies (Stresemann and Stresemann 1966), but how and why
different species of birds have different strategies for the timing and
patterns with which they replace their feathers remains poorly known.
How selection interacts with molt, and not just feather phenotype, is an
essential question because molt is the underlying mechanism of feather
production. How molts provide limitations and opportunities for seasonal
change may be of widespread importance for understanding evolution of
avian color at a broader scale. For example, some juvenile birds are
brightly colored, and then lose this bright coloration in the highly
conserved preformative molt that occurs shortly after fledging (Pyle
2009). It may be that the preformative molt provides an opportunity for
these chicks to respond to selection from parental choice in the nest
(Lyon et al. 1994) without being ``stuck'' in a bright plumage for their
entire first year of life.

The needs for seasonal dichromatism likely vary by latitude and social
system in birds (Friedman et al. 2009, Simpson et al 2015), but these
results suggest that they may not be the primary factor influencing the
evolution of prealternate molt in the New World warblers. A major study
into global variation in seasonal plumage coloration in birds found that
seasonal color change is more uncommon than predicted by social systems
and predation risk (McQueen et al. 2019). We believe our study sheds
some light on this conundrum. From the viewpoint of the \emph{feather
wear hypothesis} , the answer to this problem is that needs for seasonal
color change alone are not strong enough to influence molt patterns in
many species, and so seasonal color change can only evolve within the
context of pre-existing molts. This is similar to how pre-existing molts
limit the phenotypic realization of plumage maturation (Rohwer and
Butcher 1988). A two-step relationship between a birds' needs for
feather color change and the response of phenotypic evolution to those
needs may not necessarily be unexpected. Selection for color and
structure on feathers likely interact in complex ways. For example,
sexual selection on feathers may act as a ``bridge'' between peaks on
natural selective landscapes for feather structure (Persons and Currie
2019). Our results provide evidence for similar ``bridges'' across
adaptive landscapes, where naturally selected molts may provide bridges
between spaces on a social selection landscape, in this case between
year-round monochromatism, and seasonal dichromatism. Further research
into the interplay between different types of selection on the evolution
of molts and plumages in birds could consider groups with disparate
social systems, as well as quantification of feather degradation. We
suggest that molt should be considered when attempting to understand the
evolution of plumages in birds.

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\textbf{Supporting Information}

\textbf{Hosted file}

\verb`image6.emf`  available at \url{https://authorea.com/users/333884/articles/459975-title-evolution-of-breeding-plumages-in-birds-a-multiple-step-pathway-to-seasonal-dichromatism-in-new-world-warblers-aves-parulidae}

Supplemental Table 1. molt, plumage, and life history scores for warbler
species included in these analyses.

Supplemental Table 2: Presence of prealternate molt and seasonal
dichromatism by species. 1= present, 0=absent, 0.5=partial, or
intraspecific variation present.

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