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.