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, Sætre 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, 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 prebasic molt, and
generates the basic plumage. In addition to the prebasic molt,
many species of birds undergo a second molt within their annual cycle,
termed the prealternate molt, which generates thealternate 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,e.g. Black-bellied Plover (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 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 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 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 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 variable needs hypothesis . Thefeather 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.